Cancer stem cells from a rare form of glioblastoma multiforme involving the neurogenic ventricular wall

Cancer Cell International

Volumn 12, Issue , 2012, Pages

  Li, Shengwen C ^a,c,d   Vu, Long T ^a,d   Ho, Hector W ^b,c   Yin, Hong Z ^c   Keschrumrus, Vic ^a   Lu, Qiang ^f   Wang, Jun ^f   Zhang, Heying ^f   Ma, Zhiwei ^e   Stover, Alexander ^a   Weiss, John H ^c   Schwartz, Philip H ^a,g   Loudon, William G ^a,b,c  

^a CHILDREN S HOSPITAL OF ORANGE COUNTY   (United States)

^b ST JOSEPH HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CALIFORNIA STATE UNIVERSITY   (United States)

^e Good Samaritan Hospital Medical Center   (United States)

^f CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain tumor stem cells; Cancer stem cells; Glioblastoma multiforme; Organotypic brain slice culture; Primary tumors

Indexed keywords

ANTINEOPLASTIC AGENT; BETA TUBULIN; CATHEPSIN B; CATHEPSIN L; CAVEOLIN 1; CAVEOLIN 2; CD133 ANTIGEN; COLLAGEN; ENTACTIN; EPHRIN B1; EPHRIN B2; EPHRIN B3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KI 67 ANTIGEN; LAMININ; MUCIN; MUCIN 18; MUCIN 24; MUSASHI; MYC PROTEIN; NESTIN; NEURAL SPECIFIC ENDOLASE; NOTCH2 RECEPTOR; NOTCH4 RECEPTOR; NUCLEOSTEMIN; PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX ATROPHY; BRAIN EDEMA; BRAIN HEMORRHAGE; CANCER ADJUVANT THERAPY; CANCER GRADING; CANCER STEM CELL; CANCER SURGERY; CAPSULA INTERNA; CARCINOGENESIS; CELL DEATH; CELL FUNCTION; CELL HYPERPLASIA; CELL RENEWAL; CELL STRUCTURE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CYTOPLASM; EX VIVO STUDY; GLIOBLASTOMA; HISTOLOGY; HUMAN; HUMAN CELL; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IN VITRO STUDY; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; MITOSIS; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; POSTOPERATIVE PERIOD; PROTEIN EXPRESSION; SPINDLE CELL; SUBVENTRICULAR ZONE; THALAMUS; TUMOR GROWTH; TUMOR RECURRENCE; TUMOR VOLUME; WHITE MATTER;

EID: 84866502725     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-12-41     Document Type: Article

References (107)

1. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol 2006, 1:97-117. 10.1146/annurev.pathol.1.110304.100043, 18039109.
2. Li SC, Loudon WG. A novel and generalizable organotypic slice platform to evaluate stem cell potential for targeting pediatric brain tumors. Cancer Cell International 2008, 8(9):1-11. 2235833, 18177496.
3. Meeske KA, Patel SK, Palmer SN, Nelson MB, Parow AM. Factors associated with health-related quality of life in pediatric cancer survivors. Pediatr Blood Cancer 2007, 49(3):298-305. 10.1002/pbc.20923, 16779805.
4. Zebrack BJ, Gurney JG, Oeffinger K, Whitton J, Packer RJ, Mertens A, Turk N, Castleberry R, Dreyer Z, Robison LL, et al. Psychological outcomes in long-term survivors of childhood brain cancer: a report from the childhood cancer survivor study. J Clin Oncol 2004, 22(6):999-1006. 10.1200/JCO.2004.06.148, 15020603.
5. Singh S, Dirks PB. Brain tumor stem cells: identification and concepts. Neurosurg Clin N Am 2007, 18(1):31-38. viii, 10.1016/j.nec.2006.10.014, 17244552.
6. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001, 414(6859):105-111. 10.1038/35102167, 11689955.
7. Dirks PB. Brain tumour stem cells: the undercurrents of human brain cancer and their relationship to neural stem cells. Philos Trans R Soc Lond B Biol Sci 2008, 363(1489):139-152. 10.1098/rstb.2006.2017, 2605491, 17309866.
8. Tan BT, Park CY, Ailles LE, Weissman IL. The cancer stem cell hypothesis: a work in progress. Lab Invest 2006, 86(12):1203-1207. 10.1038/labinvest.3700488, 17075578.
9. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008, 456(7222):593-598. 10.1038/nature07567, 2597380, 19052619.
10. Kennedy JA, Barabe F, Poeppl AG, Wang JC, Dick JE. Comment on "Tumor growth need not be driven by rare cancer stem cells". Science 2007, 318(5857):1722. author reply 1722.
11. Adams JM, Kelly PN, Dakic A, Carotta S, Nutt SL, Strasser A. Role of "cancer stem cells" and cell survival in tumor development and maintenance. Cold Spring Harb Symp Quant Biol 2008, 73:451-459. 10.1101/sqb.2008.73.004, 19022754.
12. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science 2007, 317(5836):337. 10.1126/science.1142596, 17641192.
13. Li SC, Loudon WG. Stem Cell Therapy for Paediatric Malignant Brain Tumours: The Silver Bullet?. ONcology News (UK), June-July 2008, ISSN 1751-4975 2008, 3(1):10-14. http://www.oncologynews.biz/pdf/jun_jul_08/ONJJ08_stemcell.pdf (Accessed May 14, 2008).
14. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. ProcNatlAcadSciUSA 2000, 97(23):12846-12851.
15. Aboody KS, Najbauer J, Danks MK. Stem and progenitor cell-mediated tumor selective gene therapy. Gene Ther 2008, 15(10):739-752. 10.1038/gt.2008.41, 18369324.
16. Abel TW, Clark C, Bierie B, Chytil A, Aakre M, Gorska A, Moses HL. GFAP-Cre-mediated activation of oncogenic K-ras results in expansion of the subventricular zone and infiltrating glioma. Mol Cancer Res 2009, 7(5):645-653. 10.1158/1541-7786.MCR-08-0477, 3406747, 19435821.
17. Duntsch C, Zhou Q, Weimar JD, Frankel B, Robertson JH, Pourmotabbed T. Up-regulation of neuropoiesis generating glial progenitors that infiltrate rat intracranial glioma. J Neurooncol 2005, 71(3):245-255. 10.1007/s11060-004-2156-6, 15735912.
18. Fujita M, Sato M, Nakamura M, Kudo K, Nagasaka T, Mizuno M, Amano E, Okamoto Y, Hotta Y, Hatano H, et al. Multicentric atypical teratoid/rhabdoid tumors occurring in the eye and fourth ventricle of an infant: case report. J Neurosurg 2005, 102(3 Suppl):299-302.
19. Morota N, Deletis V, Epstein FJ, Kofler M, Abbott R, Lee M, Ruskin K. Brain stem mapping: neurophysiological localization of motor nuclei on the floor of the fourth ventricle. Neurosurgery 1995, 37(5):922-929. discussion 929-930, 10.1227/00006123-199511000-00011, 8559341.
20. Phi JH, Park SH, Chae JH, Hong KH, Park SS, Kang JH, Jun JK, Cho BK, Wang KC, Kim SK. Congenital subependymal giant cell astrocytoma: clinical considerations and expression of radial glial cell markers in giant cells. Childs Nerv Syst 2008, 24(12):1499-1503. 10.1007/s00381-008-0681-x, 18629509.
21. Stecca B, Ruiz i Altaba A. Brain as a paradigm of organ growth: Hedgehog-Gli signaling in neural stem cells and brain tumors. J Neurobiol 2005, 64(4):476-490. 10.1002/neu.20160, 16041742.
22. Uchida K, Mukai M, Okano H, Kawase T. Possible oncogenicity of subventricular zone neural stem cells: case report. Neurosurgery 2004, 55(4):977-978. 10.1227/01.NEU.0000137891.99542.43, 15458607.
23. Yano H, Ohe N, Shinoda J, Yoshimura S, Iwama T. Immunohistochemical study concerning the origin of neurocytoma-a case report. Pathol Oncol Res 2009, 15(2):301-305. 10.1007/s12253-008-9106-0, 18802789.
24. Li SC, Jin Y, Loudon WG, Song Y, Ma Z, Weiner LP, Zhong JF. From the Cover: Increase developmental plasticity of human keratinocytes with gene suppression. Proc Natl Acad Sci U S A 2011, 108(31):12793-12798. 10.1073/pnas.1100509108, 3150912, 21768375.
25. Li SC, Lee KL, Luo J, Zhong JF, Loudon WG. Convergence of normal stem cell and cancer stem cell developmental stage: Implication for differential therapies. World J Stem Cells 2011, 3(9):83-88. 10.4252/wjsc.v3.i9.83, 3192222, 22007273.
26. Li SC, Lee KL, Luo J. Control dominating subclones for managing cancer progression and posttreatment recurrence by subclonal switchboard signal: implication for new therapies. Stem Cells Dev 2012, 21(4):503-506. 10.1089/scd.2011.0267, 21933025.
27. Flanagan LA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES. Regulation of human neural precursor cells by laminin and integrins. J Neurosci Res 2006, 83(5):845-856. 10.1002/jnr.20778, 2409144, 16477652.
28. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689. 10.1016/j.cell.2006.06.044, 16923388.
29. Schwartz PH, Bryant PJ, Fuja TJ, Su H, O'Dowd DK, Klassen H. Isolation and characterization of neural progenitor cells from post-mortem human cortex. J Neurosci Res 2003, 74(6):838-851. 10.1002/jnr.10854, 14648588.
30. Li S, Seitz R, Lisanti MP. Phosphorylation of caveolin by Src tyrosine kinases: The à-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem 1996, 271:3863-3868. 10.1074/jbc.271.7.3863, 8632005.
31. Dirks PB, Fogarty MP, Emmenegger BA, Grasfeder LL, Oliver TG, Wechsler-Reya RJ. Brain tumour stem cells: the undercurrents of human brain cancer and their relationship to neural stem cells. Fibroblast growth factor blocks Sonic hedgehog signaling in neuronal precursors and tumor cells. Philos Trans R Soc Lond B Biol Sci 2007, 19(8):19.
32. Sanai N, Varez-Buylla A, Berger MS. Neural stem cells and the origin of gliomas. N Engl J Med 2005, 353(8):811-822. 10.1056/NEJMra043666, 16120861.
33. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene 2004, 23(43):7267-7273. 10.1038/sj.onc.1207946, 15378086.
34. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 2003, 100(25):15178-15183. 10.1073/pnas.2036535100, 299944, 14645703.
35. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004, 23(58):9392-9400. 10.1038/sj.onc.1208311, 15558011.
36. Dirks PB. Cancer: stem cells and brain tumours. Nature 2006, 444(7120):687-688. 10.1038/444687a, 17151644.
37. Tunici P, Irvin D, Liu G, Yuan X, Zhaohui Z, Ng H, Yu JS. Brain tumor stem cells: new targets for clinical treatments?. Neurosurg Focus 2006, 20(4):E27. 10.3171/foc.2006.20.4.17, 16709033.
38. Xu Q, Liu G, Yuan X, Xu M, Wang H, Ji J, Konda B, Black KL, Yu JS. Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens. Stem Cells 2009, 27(8):1734-1740. 10.1002/stem.102, 19536809.
39. Yu JJ, Sun X, Yuan X, Lee JW, Snyder EY, Yu JS. Immunomodulatory neural stem cells for brain tumour therapy. Expert Opin Biol Ther 2006, 6(12):1255-1262. 10.1517/14712598.6.12.1255, 17223735.
40. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, de Tribolet N, Regli L, Wick W, Kouwenhoven MC, et al. Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 2008, 26(18):3015-3024. 10.1200/JCO.2007.15.7164, 18565887.
41. Strojnik T, Rosland GV, Sakariassen PO, Kavalar R, Lah T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol 2007, 68(2):133-143. discussion 143-134, 10.1016/j.surneu.2006.10.050, 17537489.
42. Kavsan V, Shostak K, Dmitrenko V, Zozulya Y, Rozumenko V, Demotes-Mainard J. Characterization of genes with increased expression in human glioblastomas. Tsitol Genet 2005, 39(6):37-49.
43. Heimberger AB, McGary EC, Suki D, Ruiz M, Wang H, Fuller GN, Bar-Eli M. Loss of the AP-2alpha transcription factor is associated with the grade of human gliomas. Clin Cancer Res 2005, 11(1):267-272.
44. Grzybicki DM, Moore SA. Implications of prognostic markers in brain tumors. Clin Lab Med 1999, 19(4):833-847.
45. Jennings MT, Kaariainen IT, Gold L, Maciunas RJ, Commers PA. TGF beta 1 and TGF beta 2 are potential growth regulators for medulloblastomas, primitive neuroectodermal tumors, and ependymomas: evidence in support of an autocrine hypothesis. Hum Pathol 1994, 25(5):464-475. 10.1016/0046-8177(94)90118-X, 8200640.
46. Mastronardi L, Guiducci A, Puzzilli F, Ruggeri A. Relationship between Ki-67 labeling index and survival in high-grade glioma patients treated after surgery with tamoxifen. J Neurosurg Sci 1999, 43(4):263-270.
47. Sampath P, Weaver CE, Sungarian A, Cortez S, Alderson L, Stopa EG. Cerebrospinal fluid (vascular endothelial growth factor) and serologic (recoverin) tumor markers for malignant glioma. Cancer Control 2004, 11(3):174-180.
48. Schiebe M, Ohneseit P, Hoffmann W, Meyermann R, Rodemann HP, Bamberg M. Analysis of mdm2 and p53 gene alterations in glioblastomas and its correlation with clinical factors. J Neurooncol 2000, 49(3):197-203. 10.1023/A:1006410702284, 11212898.
49. Tada K, Shiraishi S, Kamiryo T, Nakamura H, Hirano H, Kuratsu J, Kochi M, Saya H, Ushio Y. Analysis of loss of heterozygosity on chromosome 10 in patients with malignant astrocytic tumors: correlation with patient age and survival. J Neurosurg 2001, 95(4):651-659. 10.3171/jns.2001.95.4.0651, 11596960.
50. Xin W, Paulino AF. Prognostic factors in malignant mixed tumors of the salivary gland: correlation of immunohistochemical markers with histologic classification. Ann Diagn Pathol 2002, 6(4):205-210. 10.1053/adpa.2002.34728, 12170450.
51. Das S, Srikanth M, Kessler JA. Cancer stem cells and glioma. Nat Clin Pract Neurol 2008, 4(8):427-435.
52. Bonavia R, Inda MM, Cavenee WK, Furnari FB. Heterogeneity maintenance in glioblastoma: a social network. Cancer Res 2011, 71(12):4055-4060. 10.1158/0008-5472.CAN-11-0153, 3117065, 21628493.
53. Qiang L, Yang Y, Ma YJ, Chen FH, Zhang LB, Liu W, Qi Q, Lu N, Tao L, Wang XT, et al. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett 2009, 279(1):13-21. 10.1016/j.canlet.2009.01.016, 19232461.
54. Huttner HB, Janich P, Kohrmann M, Jaszai J, Siebzehnrubl F, Blumcke I, Suttorp M, Gahr M, Kuhnt D, Nimsky C, et al. The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying central nervous system disease. Stem Cells 2008, 26(3):698-705. 10.1634/stemcells.2007-0639, 18096722.
55. Cheng JX, Liu BL, Zhang X. How powerful is CD133 as a cancer stem cell marker in brain tumors?. Cancer Treat Rev 2009,
56. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, Lichter P, Unterberg A, Radlwimmer B, Herold-Mende CC. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 2008, 14(1):123-129. 10.1158/1078-0432.CCR-07-0932, 18172261.
57. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003, 63(18):5821-5828.
58. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004, 432(7015):396-401. 10.1038/nature03128, 15549107.
59. Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE, Nuber UA. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res 2007, 67(12):5727-5736. 10.1158/0008-5472.CAN-07-0183, 17575139.
60. 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(19):7011-7021. 10.1158/0008-5472.CAN-04-1364, 15466194.
61. Lathia JD, Gallagher J, Myers JT, Li M, Vasanji A, McLendon RE, Hjelmeland AB, Huang AY, Rich JN. Direct in vivo evidence for tumor propagation by glioblastoma cancer stem cells. PLoS One 2011, 6(9):e24807. 10.1371/journal.pone.0024807, 3178553, 21961046.
62. Shu Q, Wong KK, Su JM, Adesina AM, Yu LT, Tsang YT, Antalffy BC, Baxter P, Perlaky L, Yang J, et al. Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells 2008, 26(6):1414-1424. 10.1634/stemcells.2007-1009, 18403755.
63. Gong X, Schwartz PH, Linskey ME, Bota DA. Neural stem/progenitors and glioma stem-like cells have differential sensitivity to chemotherapy. Neurology 2011, 76(13):1126-1134. 10.1212/WNL.0b013e318212a89f, 3269770, 21346220.
64. Kamoun WS, Ley CD, Farrar CT, Duyverman AM, Lahdenranta J, Lacorre DA, Batchelor TT, di Tomaso E, Duda DG, Munn LL, et al. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J Clin Oncol 2009, 27(15):2542-2552. 10.1200/JCO.2008.19.9356, 2739611, 19332720.
65. Zajc I, Hreljac I, Lah T. Cathepsin L affects apoptosis of glioblastoma cells: a potential implication in the design of cancer therapeutics. Anticancer Res 2006, 26(5A):3357-3364.
66. Steinert PM, Liem RKH. Intermediate filament dynamics. Cell (Cambridge) 1990, 60(4):521-523.
67. Shih AH, Holland EC. Notch signaling enhances nestin expression in gliomas. Neoplasia 2006, 8(12):1072-1082. 10.1593/neo.06526, 1790729, 17217625.
68. Strojnik T, Røsland GV, Sakariassen PO, Kavalar R, Lah T. Neural stem cell markers, nestin and musashi proteins, in the progression of human glioma: correlation of nestin with prognosis of patient survival. Surg Neurol 2007, 68(2):133-143. 10.1016/j.surneu.2006.10.050, 17537489.
69. Rooprai HK, McCormick D. Proteases and their inhibitors in human brain tumours: a review. Anticancer Res 1997, 17(6B):4151-4162.
70. Levicar N, Nuttall RK, Lah TT. Proteases in brain tumour progression. Acta Neurochir (Wien) 2003, 145(9):825-838.
71. Ezhilarasan R, Mohanam I, Govindarajan K, Mohanam S. Glioma cells suppress hypoxia-induced endothelial cell apoptosis and promote the angiogenic process. Int J Oncol 2007, 30(3):701-707. 2435071, 17273772.
72. Guo P, Imanishi Y, Cackowski FC, Jarzynka MJ, Tao HQ, Nishikawa R, Hirose T, Hu B, Cheng SY. Up-regulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am J Pathol 2005, 166(3):877-890. 10.1016/S0002-9440(10)62308-5, 1602359, 15743799.
73. Hu B, Guo P, Fang Q, Tao HQ, Wang D, Nagane M, Huang HJ, Gunji Y, Nishikawa R, Alitalo K, et al. Angiopoietin-2 induces human glioma invasion through the activation of matrix metalloprotease-2. Proc Natl Acad Sci U S A 2003, 100(15):8904-8909. 10.1073/pnas.1533394100, 166411, 12861074.
74. Hu B, Jarzynka MJ, Guo P, Imanishi Y, Schlaepfer DD, Cheng SY. Angiopoietin 2 induces glioma cell invasion by stimulating matrix metalloprotease 2 expression through the alphavbeta1 integrin and focal adhesion kinase signaling pathway. Cancer Res 2006, 66(2):775-783. 10.1158/0008-5472.CAN-05-1149, 2868063, 16424009.
75. Wong ET, Alsop D, Lee D, Tam A, Barron L, Bloom J, Gautam S, Wu JK. Cerebrospinal fluid matrix metalloproteinase-9 increases during treatment of recurrent malignant gliomas. Cerebrospinal Fluid Res 2008, 5:1. 10.1186/1743-8454-5-1, 2263020, 18186943.
76. Sivaparvathi M, Yamamoto M, Nicolson GL, Gokaslan ZL, Fuller GN, Liotta LA, Sawaya R, Rao JS. Expression and immunohistochemical localization of cathepsin L during the progression of human gliomas. Clin Exp Metastasis 1996, 14(1):27-34. 10.1007/BF00157683, 8521613.
77. Levicar N, Dewey RA, Daley E, Bates TE, Davies D, Kos J, Pilkington GJ, Lah TT. Selective suppression of cathepsin L by antisense cDNA impairs human brain tumor cell invasion in vitro and promotes apoptosis. Cancer Gene Ther 2003, 10(2):141-151. 10.1038/sj.cgt.7700546, 12536203.
78. Strojnik T, Zidanik B, Kos J, Lah TT. Cathepsins B and L are markers for clinically invasive types of meningiomas. Neurosurgery 2001, 48(3):598-605. 10.1097/00006123-200103000-00029, 11270551.
79. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 1991, 65(5):737-752. 10.1016/0092-8674(91)90382-9, 1904008.
80. Haupt Y, Bath ML, Harris AW, Adams JM. bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene 1993, 8(11):3161-3164.
81. Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G, Raychaudhury A, Newton HB, Chiocca EA, Lawler S. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 2008, 68(22):9125-9130. 10.1158/0008-5472.CAN-08-2629, 19010882.
82. Martin S, Cosset EC, Terrand J, Maglott A, Takeda K, Dontenwill M. Caveolin-1 regulates glioblastoma aggressiveness through the control of alpha(5)beta(1) integrin expression and modulates glioblastoma responsiveness to SJ749, an alpha(5)beta(1) integrin antagonist. Biochim Biophys Acta 2009, 1793(2):354-367. 10.1016/j.bbamcr.2008.09.019, 18992284.
83. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, Hansen SH, Nishimoto I, Lisanti MP. Evidence for a regulated interaction of hetero-trimeric G proteins with caveolin. J Biol Chem 1995, 270(26):15693-15701. 10.1074/jbc.270.26.15693, 7797570.
84. Li S, Song KS, Lisanti MP. Expression and characterization of recombinant caveolin: Purification by poly-histidine tagging and cholesterol-dependent incorporation into defined lipid membranes. JBiolChem 1996, 271:568-573.
85. Lisanti MP, Scherer P, Tang ZL, Sargiacomo M. Caveolae, caveolin and caveolin-rich membrane domains: A signalling hypothesis. Trends Cell Biol 1994, 4:231-235. 10.1016/0962-8924(94)90114-7, 14731661.
86. Tahir SA, Ren C, Timme TL, Gdor Y, Hoogeveen R, Morrisett JD, Frolov A, Ayala G, Wheeler TM, Thompson TC. Development of an Immunoassay for Serum Caveolin-1 A Novel Biomarker for Prostate Cancer 1 2003, 3653-3659.
87. Tahir SA, Frolov A, Hayes TG, Mims MP, Miles BJ, Lerner SP, Wheeler TM, Ayala G, Thompson TC, Kadmon D. Preoperative serum caveolin-1 as a prognostic marker for recurrence in a radical prostatectomy cohort. Clin Cancer Res 2006, 12(16):4872-4875. 10.1158/1078-0432.CCR-06-0417, 16914574.
88. Witkiewicz AK, Dasgupta A, Sotgia F, Mercier I, Pestell RG, Sabel M, Kleer CG, Brody JR, Lisanti MP. An Absence of Stromal Caveolin-1 Expression Predicts Early Tumor Recurrence and Poor Clinical Outcome in Human Breast Cancers. Am J Pathol 2009,
89. Piccirillo SG, Combi R, Cajola L, Patrizi A, Redaelli S, Bentivegna A, Baronchelli S, Maira G, Pollo B, Mangiola A, et al. Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution. Oncogene 2009, 28(15):1807-1811. 10.1038/onc.2009.27, 19287454.
90. Li SC, Han YP, Dethlefs BA, Loudon WG. Therapeutic Window, a Critical Developmental Stage for Stem Cell Therapies. Curr Stem Cell Res Ther 2010,
91. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17(1):98-110. 10.1016/j.ccr.2009.12.020, 2818769, 20129251.
92. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 2012, 483(7390):479-483. 10.1038/nature10866, 3351699, 22343889.
93. Feng J, Kim ST, Liu W, Kim JW, Zhang Z, Zhu Y, Berens M, Sun J, Xu J. An integrated analysis of germline and somatic, genetic and epigenetic alterations at 9p21.3 in glioblastoma. Cancer 2012, 118(1):232-240. 10.1002/cncr.26250, 21713760.
94. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4(6):568-580. 10.1016/j.stem.2009.03.014, 19497285.
95. Loring JF, Wesselschmidt RL, Schwartz PH. Human Stem Cell Manual: A Laboratory Guide 2007, Academic Press.
96. Nethercott H, Maxwell H, Schwartz PH. Neural progenitor cell culture. Human stem cell manual: A laboratory guide 2007, 309-331. Boston, London, New York: Academic Press, Elsevier, Loring JF, Wesselschmidt RL, Schwartz PH.
97. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De VS, Fiocco R, Foroni C, Dimeco F, Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004, 64(19):7011-7021. 10.1158/0008-5472.CAN-04-1364, 15466194.
98. Grimm EA, Loudon WG. The generation and quantitation of cell-mediated cytotoxicity. Cytokines: A practical approach 1995, 197-214. Oxford: IRL Press, Balkwill FR, 2.
99. Berglund DL, Taffs RE, Robertson NP. A rapid analytical technique for flow cytometric analysis of cell viability using calcofluor white M2R. Cytometry 1987, 8(4):421-426. 10.1002/cyto.990080412, 3304880.
100. Diaz TM, Pertega S, Ortega D, Lopez E, Centeno A, Manez R, Domenech N. FDA/PI flow cytometry assay of complement-mediated cytotoxicity of antibodies generated during xenotransplantation. Cytometry A 2004, 62(1):54-60.
101. Saha NR, Usami T, Suzuki Y. A double staining flow cytometric assay for the detection of steroid induced apoptotic leucocytes in common carp (Cyprinus carpio). Dev Comp Immunol 2003, 27(5):351-363. 10.1016/S0145-305X(02)00116-7, 12631518.
102. Koleske AJ, Baltimore D, Lisanti MP. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 1995, 92(1381-1385).
103. Yin HZ, Sensi SL, Carriedo SG, Weiss JH. Dendritic localization of Ca(2+)-permeable AMPA/kainate channels in hippocampal pyramidal neurons. J Comp Neurol 1999, 409(2):250-260. 10.1002/(SICI)1096-9861(19990628)409:2<250::AID-CNE6>3.0.CO;2-Y, 10379918.
104. Li S, Kirov I, Klassen HK, Schwartz PH. Characterization of stem cells using reverse transcriptase polymerase chain reaction. Human stem cell manual: a laboratory guide 2007, 127-148. Boston, New York, London: Academic Press, Elsevier, Loring JF, Wesselschmidt RL, Schwartz PH.
105. Flanagan LA, Ziaeian B, Palmer T, Schwartz PH. Immunocytochemical analysis of stem cells. Human Stem Cell Manual: A Laboratory Guide 2007, 108-126. Boston, New York: Academic Press, Elsevier, Loring JF, Wesselschmidt RL, Schwartz PH.
106. Ju X, Katiyar S, Wang C, Liu M, Jiao X, Li S, Zhou J, Turner J, Lisanti MP, Russell RG, et al. Akt1 governs breast cancer progression in vivo. Proc Natl Acad Sci U S A 2007, 104(18):7438-7443. 10.1073/pnas.0605874104, 1863437, 17460049.
107. Li S, Couet J, Lisanti MP. Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 1996, 271(46):29182-29190. 10.1074/jbc.271.46.29182, 8910575.