Mouse low-grade gliomas contain cancer stem cells with unique molecular and functional properties

Cell Reports

Volumn 10, Issue 11, 2015, Pages 1899-1912

  Chen, Yi Hsien ^a   McGowan, LucyD'Agostino ^a   Cimino, Patrick J ^a   Dahiya, Sonika ^a   Leonard, Jeffrey R ^a   Lee, DaYong ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER G1; CARBOPLATIN; CD133 ANTIGEN; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; NEUROFIBROMIN; RAPAMYCIN; TEMOZOLOMIDE; VINCRISTINE; ABC TRANSPORTER; ABCG1 PROTEIN, MOUSE; ANTINEOPLASTIC AGENT; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; LIPOPROTEIN; PEPTIDE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CANCER STEM CELL; CELL SURVIVAL; CONTROLLED STUDY; DRUG SENSITIVITY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NEURAL STEM CELL; NONHUMAN; OPTIC NERVE GLIOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; ANIMAL; BRAIN TUMOR; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; GLIOMA; METABOLISM; PATHOLOGY;

ANIMALS; ANTIGENS, CD; ANTINEOPLASTIC AGENTS; APOPTOSIS; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN NEOPLASMS; CELLS, CULTURED; DRUG RESISTANCE, NEOPLASM; ENDOPLASMIC RETICULUM STRESS; GLIOMA; GLYCOPROTEINS; HUMANS; LIPOPROTEINS; MICE; MICE, INBRED C57BL; NEOPLASTIC STEM CELLS; NEUROFIBROMIN 1; PEPTIDES; TRANSCRIPTOME;

EID: 84925609179     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.041     Document Type: Article

References (73)

1. Bajenaru M.L., Hernandez M.R., Perry A., Zhu Y., Parada L.F., Garbow J.R., Gutmann D.H. Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res. 2003, 63:8573-8577.
2. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
3. Beier D., Schulz J.B., Beier C.P. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol. Cancer 2011, 10:128.
4. Bleau A.M., Hambardzumyan D., Ozawa T., Fomchenko E.I., Huse J.T., Brennan C.W., Holland E.C. 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. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
6. Booth L., Roberts J.L., Cruickshanks N., Grant S., Poklepovic A., Dent P. Regulation of OSU-03012 toxicity by ER stress proteins and ER stress-inducing drugs. Mol. Cancer Ther. 2014, 13:2384-2398.
7. Carrière A., Cargnello M., Julien L.A., Gao H., Bonneil E., Thibault P., Roux P.P. Oncogenic MAPK signaling stimulates mTORC1 activity by promoting RSK-mediated raptor phosphorylation. Curr. Biol. 2008, 18:1269-1277.
8. Chen J., Li Y., Yu T.S., McKay R.M., Burns D.K., Kernie S.G., Parada L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488:522-526.
9. Cho H.Y., Wang W., Jhaveri N., Lee D.J., Sharma N., Dubeau L., Schönthal A.H., Hofman F.M., Chen T.C. NEO212, temozolomide conjugated to perillyl alcohol, is a novel drug for effective treatment of a broad range of temozolomide-resistant gliomas. Mol. Cancer Ther. 2014, 13:2004-2017.
10. Ciechomska I.A., Gabrusiewicz K., Szczepankiewicz A.A., Kaminska B. Endoplasmic reticulum stress triggers autophagy in malignant glioma cells undergoing cyclosporine a-induced cell death. Oncogene 2013, 32:1518-1529.
11. Daginakatte G.C., Gutmann D.H. Neurofibromatosis-1 (Nf1) heterozygous brain microglia elaborate paracrine factors that promote Nf1-deficient astrocyte and glioma growth. Hum. Mol. Genet. 2007, 16:1098-1112.
12. Dasgupta B., Gutmann D.H. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation invitro and invivo. J.Neurosci. 2005, 25:5584-5594.
13. Erbay E., Babaev V.R., Mayers J.R., Makowski L., Charles K.N., Snitow M.E., Fazio S., Wiest M.M., Watkins S.M., Linton M.F., Hotamisligil G.S. Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 2009, 15:1383-1391.
14. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
15. Golebiewska A., Bougnaud S., Stieber D., Brons N.H., Vallar L., Hertel F., Klink B., Schröck E., Bjerkvig R., Niclou S.P. Side population in human glioblastoma is non-tumorigenic and characterizes brain endothelial cells. Brain 2013, 136:1462-1475.
16. Guillamo J.S., Créange A., Kalifa C., Grill J., Rodriguez D., Doz F., Barbarot S., Zerah M., Sanson M., Bastuji-Garin S., Wolkenstein P. Prognostic factors of CNS tumours in Neurofibromatosis 1 (NF1): a retrospective study of 104 patients. Brain 2003, 126:152-160. Réseau NF France.
17. Hale J.S., Otvos B., Sinyuk M., Alvarado A.G., Hitomi M., Stoltz K., Wu Q., Flavahan W., Levison B., Johansen M.L., et al. Cancer stem cell-specific scavenger receptor 36 drives glioblastoma progression. Stem Cells 2014, 32:1746-1758.
18. Hegedus B., Banerjee D., Yeh T.H., Rothermich S., Perry A., Rubin J.B., Garbow J.R., Gutmann D.H. Preclinical cancer therapy in a mouse model of neurofibromatosis-1 optic glioma. Cancer Res. 2008, 68:1520-1528.
19. Hegedus B., Hughes F.W., Garbow J.R., Gianino S., Banerjee D., Kim K., Ellisman M.H., Brantley M.A., Gutmann D.H. Optic nerve dysfunction in a mouse model of neurofibromatosis-1 optic glioma. J.Neuropathol. Exp. Neurol. 2009, 68:542-551.
20. Hope K.J., Jin L., Dick J.E. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol. 2004, 5:738-743.
21. Horiguchi S., Takahashi J., Kishi Y., Morizane A., Okamoto Y., Koyanagi M., Tsuji M., Tashiro K., Honjo T., Fujii S., Hashimoto N. Neural precursor cells derived from human embryonic brain retain regional specificity. J.Neurosci. Res. 2004, 75:817-824.
22. Johnson G.G., White M.C., Wu J.H., Vallejo M., Grimaldi M. The deadly connection between endoplasmic reticulum, Ca2+, protein synthesis, and the endoplasmic reticulum stress response in malignant glioma cells. Neuro-oncol. 2014, 16:1086-1099.
23. Kaul A., Chen Y.H., Emnett R.J., Dahiya S., Gutmann D.H. Pediatric glioma-associated KIAA1549:BRAF expression regulates neuroglial cell growth in a cell type-specific and mTOR-dependent manner. Genes Dev. 2012, 26:2561-2566.
24. Kennedy M.A., Barrera G.C., Nakamura K., Baldán A., Tarr P., Fishbein M.C., Frank J., Francone O.L., Edwards P.A. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 2005, 1:121-131.
25. Kim C.F., Jackson E.L., Woolfenden A.E., Lawrence S., Babar I., Vogel S., Crowley D., Bronson R.T., Jacks T. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005, 121:823-835.
26. Kim H.T., Kim I.S., Lee I.S., Lee J.P., Snyder E.Y., Park K.I. Human neurospheres derived from the fetal central nervous system are regionally and temporally specified but are not committed. Exp. Neurol. 2006, 199:222-235.
27. Kim K.Y., Ju W.K., Hegedus B., Gutmann D.H., Ellisman M.H. Ultrastructural characterization of the optic pathway in a mouse model of neurofibromatosis-1 optic glioma. Neuroscience 2010, 170:178-188.
28. Klucken J., Büchler C., Orsó E., Kaminski W.E., Porsch-Ozcürümez M., Liebisch G., Kapinsky M., Diederich W., Drobnik W., Dean M., et al. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc. Natl. Acad. Sci. USA 2000, 97:817-822.
29. Kwiatkowski D.J., Zhang H., Bandura J.L., Heiberger K.M., Glogauer M., el-Hashemite N., Onda H. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet. 2002, 11:525-534.
30. Lathia J.D., Gallagher J., Heddleston J.M., Wang J., Eyler C.E., Macswords J., Wu Q., Vasanji A., McLendon R.E., Hjelmeland A.B., Rich J.N. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010, 6:421-432.
31. Lathia J.D., Li M., Sinyuk M., Alvarado A.G., Flavahan W.A., Stoltz K., Rosager A.M., Hale J., Hitomi M., Gallagher J., et al. High-throughput flow cytometry screening reveals a role for junctional adhesion molecule a as a cancer stem cell maintenance factor. Cell Rep. 2014, 6:117-129.
32. Lee Y., Yeh T.H., Emnett R.J., White C.R., Gutmann D.H. Neurofibromatosis-1 regulates neuroglial progenitor proliferation and glial differentiation in a brain region-specific manner. Genes Dev. 2010, 24:2317-2329.
33. Lee Y., Gianino S.M., Gutmann D.H. Innate neural stem cell heterogeneity determines the patterning of glioma formation in children. Cancer Cell 2012, 22:131-138.
34. Li J., Lee A.S. Stress induction of GRP78/BiP and its role in cancer. Curr. Mol. Med. 2006, 6:45-54.
35. Lito P., Saborowski A., Yue J., Solomon M., Joseph E., Gadal S., Saborowski M., Kastenhuber E., Fellmann C., Ohara K., et al. Disruption of CRAF-mediated MEK activation is required for effective MEK inhibition in KRAS mutant tumors. Cancer Cell 2014, 25:697-710.
36. Liu H., Bowes R.C., van de Water B., Sillence C., Nagelkerke J.F., Stevens J.L. Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+ disturbances, and cell death in renal epithelial cells. J.Biol. Chem. 1997, 272:21751-21759.
37. Liu G., Yuan X., Zeng Z., Tunici P., Ng H., Abdulkadir I.R., Lu L., Irvin D., Black K.L., Yu J.S. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol. Cancer 2006, 5:67.
38. Liu W.T., Huang C.Y., Lu I.C., Gean P.W. Inhibition of glioma growth by minocycline is mediated through endoplasmic reticulum stress-induced apoptosis and autophagic cell death. Neuro-oncol. 2013, 15:1127-1141.
39. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
40. Luo B., Lee A.S. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013, 32:805-818.
41. Ma L., Chen Z., Erdjument-Bromage H., Tempst P., Pandolfi P.P. Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 2005, 121:179-193.
42. Mahoney D.H., Cohen M.E., Friedman H.S., Kepner J.L., Gemer L., Langston J.W., James H.E., Duffner P.K., Kun L.E. Carboplatin is effective therapy for young children with progressive optic pathway tumors: a Pediatric Oncology Group phase II study. Neuro-oncol. 2000, 2:213-220.
43. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 2002, 10:151-162.
44. Nakata S., Campos B., Bageritz J., Bermejo J.L., Becker N., Engel F., Acker T., Momma S., Herold-Mende C., Lichter P., et al. LGR5 is a marker of poor prognosis in glioblastoma and is required for survival of brain cancer stem-like cells. Brain Pathol. 2013, 23:60-72.
45. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Görgün C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
46. Pace A., Vidiri A., Galiè E., Carosi M., Telera S., Cianciulli A.M., Canalini P., Giannarelli D., Jandolo B., Carapella C.M. Temozolomide chemotherapy for progressive low-grade glioma: clinical benefits and radiological response. Ann. Oncol. 2003, 14:1722-1726.
47. Packer R.J., Lange B., Ater J., Nicholson H.S., Allen J., Walker R., Prados M., Jakacki R., Reaman G., Needles M.N., et al. Carboplatin and vincristine for recurrent and newly diagnosed low-grade gliomas of childhood. J.Clin. Oncol. 1993, 11:850-856.
48. Packer R.J., Ater J., Allen J., Phillips P., Geyer R., Nicholson H.S., Jakacki R., Kurczynski E., Needle M., Finlay J., et al. Carboplatin and vincristine chemotherapy for children with newly diagnosed progressive low-grade gliomas. J.Neurosurg. 1997, 86:747-754.
49. Parry P.V., Engh J.A. Knockdown of LGR5 suppresses the proliferation of glioma cells invitro and invivo. Neurosurgery 2014, 74:N14-N15.
50. Pietras A., Katz A.M., Ekström E.J., Wee B., Halliday J.J., Pitter K.L., Werbeck J.L., Amankulor N.M., Huse J.T., Holland E.C. Osteopontin-CD44 signaling in the glioma perivascular niche enhances cancer stem cell phenotypes and promotes aggressive tumor growth. Cell Stem Cell 2014, 14:357-369.
51. Pong W.W., Higer S.B., Gianino S.M., Emnett R.J., Gutmann D.H. Reduced microglial CX3CR1 expression delays neurofibromatosis-1 glioma formation. Ann. Neurol. 2013, 73:303-308.
52. Raabe E.H., Lim K.S., Kim J.M., Meeker A., Mao X.G., Nikkhah G., Maciaczyk J., Kahlert U., Jain D., Bar E., et al. BRAF activation induces transformation and then senescence in human neural stem cells: a pilocytic astrocytoma model. Clin. Cancer Res. 2011, 17:3590-3599.
53. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
54. Sakariassen P.O., Immervoll H., Chekenya M. Cancer stem cells as mediators of treatment resistance in brain tumors: status and controversies. Neoplasia 2007, 9:882-892.
55. See W.L., Tan I.L., Mukherjee J., Nicolaides T., Pieper R.O. Sensitivity of glioblastomas to clinically available MEK inhibitors is defined by neurofibromin 1 deficiency. Cancer Res. 2012, 72:3350-3359.
56. 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. Cancer Res. 2003, 63:5821-5828.
57. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
58. Son M.J., Woolard K., Nam D.H., Lee J., Fine H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4:440-452.
59. Suzuki K., Gerelchuluun A., Hong Z., Sun L., Zenkoh J., Moritake T., Tsuboi K. Celecoxib enhances radiosensitivity of hypoxic glioblastoma cells through endoplasmic reticulum stress. Neuro-oncol. 2013, 15:1186-1199.
60. Tarling E.J., Edwards P.A. ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc. Natl. Acad. Sci. USA 2011, 108:19719-19724.
61. Tarling E.J., Bojanic D.D., Tangirala R.K., Wang X., Lovgren-Sandblom A., Lusis A.J., Bjorkhem I., Edwards P.A. Impaired development of atherosclerosis in Abcg1-/- Apoe-/- mice: identification of specific oxysterols that both accumulate in Abcg1-/- Apoe-/- tissues and induce apoptosis. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1174-1180.
62. Taylor M.D., Poppleton H., Fuller C., Su X., Liu Y., Jensen P., Magdaleno S., Dalton J., Calabrese C., Board J., et al. Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 2005, 8:323-335.
63. Tchoghandjian A., Fernandez C., Colin C., El Ayachi I., Voutsinos-Porche B., Fina F., Scavarda D., Piercecchi-Marti M.D., Intagliata D., Ouafik L., et al. Pilocytic astrocytoma of the optic pathway: a tumour deriving from radial glia cells with a specific gene signature. Brain 2009, 132:1523-1535.
64. Tchoghandjian A., Baeza N., Colin C., Cayre M., Metellus P., Beclin C., Ouafik L., Figarella-Branger D. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 2010, 20:211-221.
65. Vermeulen L., Todaro M., de Sousa Mello F., Sprick M.R., Kemper K., Perez Alea M., Richel D.J., Stassi G., Medema J.P. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc. Natl. Acad. Sci. USA 2008, 105:13427-13432.
66. Wang N., Lan D., Chen W., Matsuura F., Tall A.R. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. USA 2004, 101:9774-9779.
67. Wang D., Zhou J., Fan C., Jiao F., Liu B., Sun P., Miao J., Zhang Q. Knockdown of LGR5 suppresses the proliferation of glioma cells invitro and invivo. Oncol. Rep. 2014, 31:41-49.
68. Wojcik A.J., Skaflen M.D., Srinivasan S., Hedrick C.C. A critical role for ABCG1 in macrophage inflammation and lung homeostasis. J.Immunol. 2008, 180:4273-4282.
69. Xue J., Wei J., Dong X., Zhu C., Li Y., Song A., Liu Z. ABCG1 deficiency promotes endothelial apoptosis by endoplasmic reticulum stress-dependent pathway. J.Physiol. Sci. 2013, 63:435-444.
70. Yeh T.H., Lee Y., Gianino S.M., Gutmann D.H. Microarray analyses reveal regional astrocyte heterogeneity with implications for neurofibromatosis type 1 (NF1)-regulated glial proliferation. Glia 2009, 57:1239-1249.
71. Yvan-Charvet L., Ranalletta M., Wang N., Han S., Terasaka N., Li R., Welch C., Tall A.R. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J.Clin. Invest. 2007, 117:3900-3908.
72. Yvan-Charvet L., Pagler T.A., Seimon T.A., Thorp E., Welch C.L., Witztum J.L., Tabas I., Tall A.R. ABCA1 and ABCG1 protect against oxidative stress-induced macrophage apoptosis during efferocytosis. Circ. Res. 2010, 106:1861-1869.
73. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998, 12:982-995.