Journal of Korean Neurosurgical Society

  • 제63권1호
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  • Pages.26-33
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  • 2020
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  • 2005-3711(pISSN)
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  • 1598-7876(eISSN)
대한신경외과학회 (The Korean Neurosurgical Society)
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Glioblastoma Cellular Origin and the Firework Pattern of Cancer Genesis from the Subventricular Zone

  • Yoon, Seon-Jin (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Park, Junseong (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Jang, Dong-Su (Medical Research Support Services, Yonsei University College of Medicine) ;
  • Kim, Hyun Jung (Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Lee, Joo Ho (Department of Radiation Oncology, Seoul National University Hospital, Seoul National University College of Medicine) ;
  • Jo, Euna (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Choi, Ran Joo (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Shim, Jin-Kyung (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Moon, Ju Hyung (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Kim, Eui-Hyun (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Chang, Jong Hee (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine) ;
  • Lee, Jeong Ho (Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Kang, Seok-Gu (Department of Neurosurgery, Brain Tumor Center, Severance Hospital, Yonsei University College of Medicine)
  • 투고 : 2019.05.31
  • 심사 : 2019.07.01
  • 발행 : 2020.01.01
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초록

Glioblastoma (GBM) is a disease without any definite cure. Numerous approaches have been tested in efforts to conquer this brain disease, but patients invariably experience recurrence or develop resistance to treatment. New surgical tools, carefully chosen samples, and experimental methods are enabling discoveries at single-cell resolution. The present article reviews the cell-of-origin of isocitrate dehydrogenase (IDH)-wildtype GBM, beginning with the historical background for focusing on cellular origin and introducing the cancer genesis patterned on firework. The authors also review mutations associated with the senescence process in cells of the subventricular zone (SVZ), and biological validation of somatic mutations in a mouse SVZ model. Understanding GBM would facilitate research on the origin of other cancers and may catalyze the development of new management approaches or treatments against IDH-wildtype GBM.

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참고문헌

  1. Alcantara Llaguno S, Chen J, Kwon CH, Jackson EL, Li Y, Burns DK, et al. : Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15 : 45-56, 2009 https://doi.org/10.1016/j.ccr.2008.12.006
  2. Alcantara Llaguno S, Sun D, Pedraza AM, Vera E, Wang Z, Burns DK, et al. : Cell-of-origin susceptibility to glioblastoma formation declines with neural lineage restriction. Nat Neurosci 22 : 545-555, 2019 https://doi.org/10.1038/s41593-018-0333-8
  3. Alcantara Llaguno SR, Wang Z, Sun D, Chen J, Xu J, Kim E, et al. : Adult lineage-restricted cns progenitors specify distinct glioblastoma subtypes. Cancer Cell 28 : 429-440, 2015 https://doi.org/10.1016/j.ccell.2015.09.007
  4. Amirian ES, Zhou R, Wrensch MR, Olson SH, Scheurer ME, Il'yasova D, et al. : Approaching a scientific consensus on the association between allergies and glioma risk: a report from the glioma international casecontrol study. Cancer Epidemiol Biomarkers Prev 25 : 282-290, 2016 https://doi.org/10.1158/1055-9965.EPI-15-0847
  5. Andersen ZJ, Pedersen M, Weinmayr G, Stafoggia M, Galassi C, Jorgensen JT, et al. : Long-term exposure to ambient air pollution and incidence of brain tumor: the european study of cohorts for air pollution effects (escape). Neuro Oncol 20 : 420-432, 2018 https://doi.org/10.1093/neuonc/nox163
  6. Bae SH, Park MJ, Lee MM, Kim TM, Lee SH, Cho SY, et al. : Toxicity profile of temozolomide in the treatment of 300 malignant glioma patients in korea. J Korean Med Sci 29 : 980-984, 2014 https://doi.org/10.3346/jkms.2014.29.7.980
  7. Barthel FP, Wesseling P, Verhaak RGW : Reconstructing the molecular life history of gliomas. Acta Neuropathol 135 : 649-670, 2018 https://doi.org/10.1007/s00401-018-1842-y
  8. Braganza MZ, Kitahara CM, Berrington de Gonzalez A, Inskip PD, Johnson KJ, Rajaraman P : Ionizing radiation and the risk of brain and central nervous system tumors: a systematic review. Neuro Oncol 14 : 1316-1324, 2012 https://doi.org/10.1093/neuonc/nos208
  9. Brauner EV, Andersen ZJ, Andersen CE, Pedersen C, Gravesen P, Ulbak K, et al. : Residential radon and brain tumour incidence in a danish cohort. PLoS One 8 : e74435, 2013 https://doi.org/10.1371/journal.pone.0074435
  10. Bredel M : Anticancer drug resistance in primary human brain tumors. Brain Res Brain Res Rev 35 : 161-204, 2001 https://doi.org/10.1016/S0165-0173(01)00045-5
  11. Brem H, Piantadosi S, Burger PC, Walker M, Selker R, Vick NA, et al. : Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The polymer-brain tumor treatment group. Lancet 345 : 1008-1012, 1995 https://doi.org/10.1016/S0140-6736(95)90755-6
  12. Calvert AE, Chalastanis A, Wu Y, Hurley LA, Kouri FM, Bi Y, et al. : Cancer-associated idh1 promotes growth and resistance to targeted therapies in the absence of mutation. Cell Rep 19 : 1858-1873, 2017 https://doi.org/10.1016/j.celrep.2017.05.014
  13. Chen J, McKay RM, Parada LF : Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell 149 : 36-47, 2012 https://doi.org/10.1016/j.cell.2012.03.009
  14. Choi J, Lee JH, Koh I, Shim JK, Park J, Jeon JY, et al. : Inhibiting stemness and invasive properties of glioblastoma tumorsphere by combined treatment with temozolomide and a newly designed biguanide (hl156a). Oncotarget 7 : 65643-65659, 2016 https://doi.org/10.18632/oncotarget.11595
  15. Dipro S, Al-Otaibi F, Alzahrani A, Ulhaq A, Al Shail E : Turcot syndrome: a synchronous clinical presentation of glioblastoma multiforme and adenocarcinoma of the colon. Case Rep Oncol Med 2012 : 720273, 2012 https://doi.org/10.1155/2012/720273
  16. Fernandez ME, Croce S, Boutin C, Cremer H, Raineteau O : Targeted electroporation of defined lateral ventricular walls: a novel and rapid method to study fate specification during postnatal forebrain neurogenesis. Neural Dev 6 : 13, 2011 https://doi.org/10.1186/1749-8104-6-13
  17. Filley AC, Henriquez M, Dey M : Recurrent glioma clinical trial, checkmate-143: the game is not over yet. Oncotarget 8 : 91779-91794, 2017 https://doi.org/10.18632/oncotarget.21586
  18. Fine HA : The basis for current treatment recommendations for malignant gliomas. J Neurooncol 20 : 111-120, 1994 https://doi.org/10.1007/BF01052722
  19. Franceschi E, Lamberti G, Paccapelo A, Di Battista M, Genestreti G, Minichillo S, et al. : Third-line therapy in recurrent glioblastoma: is it another chance for bevacizumab? J Neurooncol 139 : 383-388, 2018 https://doi.org/10.1007/s11060-018-2873-x
  20. Friedmann-Morvinski D, Bushong EA, Ke E, Soda Y, Marumoto T, Singer O, et al. : Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338 : 1080-1084, 2012 https://doi.org/10.1126/science.1226929
  21. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. : A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 370 : 699-708, 2014 https://doi.org/10.1056/NEJMoa1308573
  22. Goffart N, Kroonen J, Rogister B : Glioblastoma-initiating cells: relationship with neural stem cells and the micro-environment. Cancers (Basel) 5 : 1049-1071, 2013 https://doi.org/10.3390/cancers5031049
  23. Inskip PD, Sigurdson AJ, Veiga L, Bhatti P, Ronckers C, Rajaraman P, et al. : Radiation-related new primary solid cancers in the childhood cancer survivor study: comparative radiation dose response and modification of treatment effects. Int J Radiat Oncol Biol Phys 94 : 800-807, 2016 https://doi.org/10.1016/j.ijrobp.2015.11.046
  24. INTERPHONE Study Group : Brain tumour risk in relation to mobile telephone use: results of the interphone international case-control study. Int J Epidemiol 39 : 675-694, 2010 https://doi.org/10.1093/ije/dyq079
  25. Jeong H, Park J, Shim JK, Lee JE, Kim NH, Kim HS, et al. : Combined treatment with 2'-hydroxycinnamaldehyde and temozolomide suppresses glioblastoma tumorspheres by decreasing stemness and invasiveness. J Neurooncol 143 : 69-77, 2019 https://doi.org/10.1007/s11060-019-03151-w
  26. Jeong TS, Yee GT : Glioblastoma in a patient with neurofibromatosis type 1: a case report and review of the literature. Brain Tumor Res Treat 2 : 36-38, 2014 https://doi.org/10.14791/btrt.2014.2.1.36
  27. Kang SG, Cheong JH, Huh YM, Kim EH, Kim SH, Chang JH : Potential use of glioblastoma tumorsphere: clinical credentialing. Arch Pharm Res 38 : 402-407, 2015 https://doi.org/10.1007/s12272-015-0564-0
  28. Kendall GM, Little MP, Wakeford R, Bunch KJ, Miles JC, Vincent TJ, et al. : A record-based case-control study of natural background radiation and the incidence of childhood leukaemia and other cancers in great britain during 1980-2006. Leukemia 27 : 3-9, 2012 https://doi.org/10.1038/leu.2012.151
  29. Khalifa J, Tensaouti F, Lusque A, Plas B, Lotterie JA, Benouaich-Amiel A, et al. : Subventricular zones: new key targets for glioblastoma treatment. Radiat Oncol 12 : 67, 2017 https://doi.org/10.1186/s13014-017-0791-2
  30. Kim EH, Lee JH, Oh Y, Koh I, Shim JK, Park J, et al. : Inhibition of glioblastoma tumorspheres by combined treatment with 2-deoxyglucose and metformin. Neuro Oncol 19 : 197-207, 2017 https://doi.org/10.1093/neuonc/now174
  31. Kim S, Alexander CM : Tumorsphere assay provides more accurate prediction of in vivo responses to chemotherapeutics. Biotechnol Lett 36 : 481-488, 2014 https://doi.org/10.1007/s10529-013-1393-1
  32. Kinnersley B, Mitchell JS, Gousias K, Schramm J, Idbaih A, Labussiere M, et al. : Quantifying the heritability of glioma using genome-wide complex trait analysis. Sci Rep 5 : 17267, 2015 https://doi.org/10.1038/srep17267
  33. 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 Oncol 11 : 281-291, 2009 https://doi.org/10.1215/15228517-2008-090
  34. Kong BH, Moon JH, Huh YM, Shim JK, Lee JH, Kim EH, et al. : Prognostic value of glioma cancer stem cell isolation in survival of primary glioblastoma patients. Stem Cells Int 2014 : 838950, 2014 https://doi.org/10.1155/2014/838950
  35. Kong BH, Park NR, Shim JK, Kim BK, Shin HJ, Lee JH, et al. : Isolation of glioma cancer stem cells in relation to histological grades in glioma specimens. Childs Nerv Syst 29 : 217-229, 2013 https://doi.org/10.1007/s00381-012-1964-9
  36. Kong BH, Shin HD, Kim SH, Mok HS, Shim JK, Lee JH, et al. : Increased in vivo angiogenic effect of glioma stromal mesenchymal stem-like cells on glioma cancer stem cells from patients with glioblastoma. Int J Oncol 42 : 1754-1762, 2013 https://doi.org/10.3892/ijo.2013.1856
  37. Kratz CP, Achatz MI, Brugieres L, Frebourg T, Garber JE, Greer MC, et al. : Cancer screening recommendations for individuals with li-fraumeni syndrome. Clin Cancer Res 23 : e38-e45, 2017 https://doi.org/10.1158/1078-0432.CCR-17-0408
  38. Kwak J, Shim JK, Kim DS, Lee JH, Choi J, Park J, et al. : Isolation and characterization of tumorspheres from a recurrent pineoblastoma patient: feasibility of a patient-derived xenograft. Int J Oncol 49 : 569-578, 2016 https://doi.org/10.3892/ijo.2016.3554
  39. Laks DR : The assessment of glioblastoma tumorspheres reveals molecular determinants of proliferation and therapeutic response. Ann Arbor : University of California, 2015, p245
  40. Lamberti G, Franceschi E, Brandes AA : The burden of oncology promises not kept in glioblastoma. Future Neurol 13 : 1-4, 2018 https://doi.org/10.2217/fnl-2017-0033
  41. Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CL, Rich JN : Cancer stem cells in glioblastoma. Genes Dev 29 : 1203-1217, 2015 https://doi.org/10.1101/gad.261982.115
  42. Lee CH, Yu CC, Wang BY, Chang WW : Tumorsphere as an effective in vitro platform for screening anti-cancer stem cell drugs. Oncotarget 7 : 1215-1226, 2015 https://doi.org/10.18632/oncotarget.6261
  43. Lee JH, Lee JE, Kahng JY, Kim SH, Park JS, Yoon SJ, et al. : Human glioblastoma arises from subventricular zone cells with low-level driver mutations. Nature 560 : 243-247, 2018 https://doi.org/10.1038/s41586-018-0389-3
  44. Lee SY : Temozolomide resistance in glioblastoma multiforme. Genes Dis 3 : 198-210, 2016 https://doi.org/10.1016/j.gendis.2016.04.007
  45. Moon JH, Kim SH, Shim JK, Roh TH, Sung KS, Lee JH, et al. : Histopathological implications of ventricle wall 5-aminolevulinic acid-induced fluorescence in the absence of tumor involvement on magnetic resonance images. Oncol Rep 36 : 837-844, 2016 https://doi.org/10.3892/or.2016.4881
  46. Neglia JP, Robison LL, Stovall M, Liu Y, Packer RJ, Hammond S, et al. : New primary neoplasms of the central nervous system in survivors of childhood cancer: a report from the childhood cancer survivor study. J Natl Cancer Inst 98 : 1528-1537, 2006 https://doi.org/10.1093/jnci/djj411
  47. Nourallah B, Digpal R, Jena R, Watts C : Irradiating the subventricular zone in glioblastoma patients: is there a case for a clinical trial? Clin Oncol (R Coll Radiol) 29 : 26-33, 2017 https://doi.org/10.1016/j.clon.2016.09.005
  48. Ostrom QT, Bauchet L, Davis FG, Deltour I, Fisher JL, Langer CE, et al. : The epidemiology of glioma in adults: a "state of the science" review. Neuro Oncol 16 : 896-913, 2014 https://doi.org/10.1093/neuonc/nou087
  49. Park J, Shim JK, Kang JH, Choi J, Chang JH, Kim SY, et al. : Regulation of bioenergetics through dual inhibition of aldehyde dehydrogenase and mitochondrial complex I suppresses glioblastoma tumorspheres. Neuro Oncol 20 : 954-965, 2018 https://doi.org/10.1093/neuonc/nox243
  50. Pearce MS, Salotti JA, Little MP, McHugh K, Lee C, Kim KP, et al. : Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 380 : 499-505, 2012 https://doi.org/10.1016/S0140-6736(12)60815-0
  51. Ramon Y Cajal Agueras S : Pio del rio-hortega: a visionary in the pathology of central nervous system tumors. Front Neuroanat 10 : 13, 2016 https://doi.org/10.3389/fnana.2016.00013
  52. Roh TH, Kang SG, Moon JH, Sung KS, Park HH, Kim SH, et al. : Survival benefit of lobectomy over gross-total resection without lobectomy in cases of glioblastoma in the noneloquent area: a retrospective study. J Neurosurg, 2019 [Epub ahead of print]
  53. Roh TH, Park HH, Kang SG, Moon JH, Kim EH, Hong CK, et al. : Longterm outcomes of concomitant chemoradiotherapy with temozolomide for newly diagnosed glioblastoma patients: a single-center analysis. Medicine (Baltimore) 96 : e7422, 2017 https://doi.org/10.1097/MD.0000000000007422
  54. Ruder AM, Carreon T, Butler MA, Calvert GM, Davis-King KE, Waters MA, et al. : Exposure to farm crops, livestock, and farm tasks and risk of glioma: the upper midwest health study. Am J Epidemiol 169 : 1479- 1491, 2009 https://doi.org/10.1093/aje/kwp075
  55. Sadetzki S, Chetrit A, Freedman L, Stovall M, Modan B, Novikov I : Longterm follow-up for brain tumor development after childhood exposure to ionizing radiation for tinea capitis. Radiat Res 163 : 424-432, 2005 https://doi.org/10.1667/RR3329
  56. Salcman M : Survival in glioblastoma: historical perspective. Neurosurgery 7 : 435-439, 1980 https://doi.org/10.1227/00006123-198011000-00001
  57. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, et al. : Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 : 740-744, 2004 https://doi.org/10.1038/nature02301
  58. Shi Y, Lim SK, Liang Q, Iyer SV, Wang HY, Wang Z, et al. : Gboxin is an oxidative phosphorylation inhibitor that targets glioblastoma. Nature 567 : 341-346, 2019 https://doi.org/10.1038/s41586-019-0993-x
  59. Shibahara I, Sonoda Y, Suzuki H, Mayama A, Kanamori M, Saito R, et al. : Glioblastoma in neurofibromatosis 1 patients without idh1, braf v600e, and tert promoter mutations. Brain Tumor Pathol 35 : 10-18, 2018 https://doi.org/10.1007/s10014-017-0302-z
  60. Sottoriva A, Kang H, Ma Z, Graham TA, Salomon MP, Zhao J, et al. : A big bang model of human colorectal tumor growth. Nat Genet 47 : 209-216, 2015 https://doi.org/10.1038/ng.3214
  61. Spiteri I, Caravagna G, Cresswell GD, Vatsiou A, Nichol D, Acar A, et al. : Evolutionary dynamics of residual disease in human glioblastoma. Ann Oncol 30 : 456-463, 2019 https://doi.org/10.1093/annonc/mdy506
  62. Stenning SP, Freedman LS, Bleehen NM : An overview of published results from randomized studies of nitrosoureas in primary high grade malignant glioma. Br J Cancer 56 : 89-90, 1987 https://doi.org/10.1038/bjc.1987.161
  63. 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 352 : 987-996, 2005 https://doi.org/10.1056/NEJMoa043330
  64. Sung KS, Shim JK, Lee JH, Kim SH, Park S, Roh TH, et al. : Success of tumorsphere isolation from who grade IV gliomas does not correlate with the weight of fresh tumor specimens: an immunohistochemical characterization of tumorsphere differentiation. Cancer Cell Int 16 : 75, 2016 https://doi.org/10.1186/s12935-016-0350-1
  65. Tabata H, Yoshinaga S, Nakajima K : Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex. Exp Brain Res 216 : 161-168, 2012 https://doi.org/10.1007/s00221-011-2933-3
  66. Tseng WL, Hsu HH, Chen Y, Tseng SH : Tumor recurrence in a glioblastoma patient after discontinuation of prolonged temozolomide treatment. Asian J Neurosurg 12 : 727-730, 2017 https://doi.org/10.4103/ajns.AJNS_39_15
  67. Walker MD, Green SB, Byar DP, Alexander E Jr, Batzdorf U, Brooks WH, et al. : Randomized comparisons of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N Engl J Med 303 : 1323-1329, 1980 https://doi.org/10.1056/NEJM198012043032303
  68. Wenger KJ, Wagner M, You SJ, Franz K, Harter PN, Burger MC, et al. : Bevacizumab as a last-line treatment for glioblastoma following failure of radiotherapy, temozolomide and lomustine. Oncol Lett 14 : 1141- 1146, 2017 https://doi.org/10.3892/ol.2017.6251
  69. Wernicke AG, Smith AW, Taube S, Mehta MP : Glioblastoma: radiation treatment margins, how small is large enough? Pract Radiat Oncol 6 : 298-305, 2016 https://doi.org/10.1016/j.prro.2015.12.002
  70. Wilson CB, Gutin P, Boldrey EB, Drafts D, Levin VA, Enot KJ : Singleagent chemotherapy of brain tumors. A five-year review. Arch Neurol 33 : 739-744, 1976 https://doi.org/10.1001/archneur.1976.00500110007002
  71. Zhu H, Acquaviva J, Ramachandran P, Boskovitz A, Woolfenden S, Pfannl R, et al. : Oncogenic egfr signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc Natl Acad Sci U S A 106 : 2712-2716, 2009 https://doi.org/10.1073/pnas.0813314106

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