A novel stem cell culture model of recurrent glioblastoma

详细信息    查看全文

• 作者：Maleeha A. Qazi ; Parvez Vora ; Chitra Venugopal…
• 关键词：GBM ; Brain tumor stem cell ; Chemotherapy ; Radiotherapy ; CD15 ; CD133
• 刊名：Journal of Neuro-Oncology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：126
• 期：1
• 页码：57-67
• 全文大小：4,116 KB
• 参考文献：1.Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O鈥橩elly M, Tamayo P, Weir BA, Gabriel S, Winckler W, Gupta S, Jakkula L, Feiler HS, Hodgson JG, James CD, Sarkaria JN, Brennan C, Kahn A, Spellman PT, Wilson RK, Speed TP, Gray JW, Meyerson M, Getz G, Perou CM, Hayes DN, Cancer Genome Atlas Research N (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17:98鈥?10. doi:10.鈥?016/鈥媕.鈥媍cr.鈥?009.鈥?2.鈥?20 PubMedCentral PubMed CrossRef
  2.Wechsler-Reya R, Scott MP (2001) The developmental biology of brain tumors. Annu Rev Neurosci 24:385鈥?28. doi:10.鈥?146/鈥媋nnurev.鈥媙euro.鈥?4.鈥?.鈥?85 PubMed CrossRef
  3.Zhu Y, Parada LF (2002) The molecular and genetic basis of neurological tumours. Nat Rev Cancer 2:616鈥?26. doi:10.鈥?038/鈥媙rc866 PubMed CrossRef
  4.Huse JT, Holland EC (2010) Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 10:319鈥?31. doi:10.鈥?038/鈥媙rc2818 PubMed CrossRef
  5.Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, EuropeanOrganisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987鈥?96. doi:10.鈥?056/鈥婲EJMoa043330 PubMed CrossRef
  6.Cancer Genome Atlas Research N (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061鈥?068. doi:10.鈥?038/鈥媙ature07385 CrossRef
  7.Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396鈥?01. doi:10.鈥?038/鈥媙ature03128 PubMed CrossRef
  8.Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821鈥?828PubMed
  9.Son MJ, Woolard K, Nam DH, Lee J, Fine HA (2009) SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4:440鈥?52. doi:10.鈥?016/鈥媕.鈥媠tem.鈥?009.鈥?3.鈥?03 PubMed CrossRef
  10.Lathia JD, Gallagher J, Heddleston JM, Wang J, Eyler CE, Macswords J, Wu Q, Vasanji A, McLendon RE, Hjelmeland AB, Rich JN (2010) Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 6:421鈥?32. doi:10.鈥?016/鈥媕.鈥媠tem.鈥?010.鈥?2.鈥?18 PubMedCentral PubMed CrossRef
  11.Bao S, Wu Q, Li Z, Sathornsumetee S, Wang H, McLendon RE, Hjelmeland AB, Rich JN (2008) Targeting cancer stem cells through L1CAM suppresses glioma growth. Cancer Res 68:6043鈥?048. doi:10.鈥?158/鈥?008-5472.鈥婥AN-08-1079 PubMedCentral PubMed CrossRef
  12.Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22:139鈥?53PubMed CrossRef
  13.Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749鈥?65PubMed CrossRef
  14.Fasano CA, Dimos JT, Ivanova NB, Lowry N, Lemischka IR, Temple S (2007) shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 1:87鈥?9. doi:10.鈥?016/鈥媕.鈥媠tem.鈥?007.鈥?4.鈥?01 PubMed CrossRef
  15.Abdouh M, Facchino S, Chatoo W, Balasingam V, Ferreira J, Bernier G (2009) BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci 29:8884鈥?896. doi:10.鈥?523/鈥婮NEUROSCI.鈥?968-09.鈥?009 PubMed CrossRef
  16.Suva ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD, Riggi N, Chi AS, Cahill DP, Nahed BV, Curry WT, Martuza RL, Rivera MN, Rossetti N, Kasif S, Beik S, Kadri S, Tirosh I, Wortman I, Shalek AK, Rozenblatt-Rosen O, Regev A, Louis DN, Bernstein BE (2014) Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 157:580鈥?94. doi:10.鈥?016/鈥媕.鈥媍ell.鈥?014.鈥?2.鈥?30 PubMedCentral PubMed CrossRef
  17.Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Molecular cancer 5:67. doi:10.鈥?186/鈥?476-4598-5-67 PubMedCentral PubMed CrossRef
  18.Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756鈥?60. doi:10.鈥?038/鈥媙ature05236 PubMed CrossRef
  19.Venugopal C, Li N, Wang X, Manoranjan B, Hawkins C, Gunnarsson T, Hollenberg R, Klurfan P, Murty N, Kwiecien J, Farrokhyar F, Provias JP, Wynder C, Singh SK (2012) Bmi1 marks intermediate precursors during differentiation of human brain tumor initiating cells. Stem Cell Res 8:141鈥?53. doi:10.鈥?016/鈥媕.鈥媠cr.鈥?011.鈥?9.鈥?08 PubMed CrossRef
  20.Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, Proescholdt M, Brawanski A, Bogdahn U, Trampe-Kieslich A, Giebel B, Wischhusen J, Reifenberger G, Hau P, Beier CP (2008) Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 68:5706鈥?715. doi:10.鈥?158/鈥?008-5472.鈥婥AN-07-6878 PubMed CrossRef
  21.Hammond LA, Eckardt JR, Baker SD, Eckhardt SG, Dugan M, Forral K, Reidenberg P, Statkevich P, Weiss GR, Rinaldi DA, Von Hoff DD, Rowinsky EK (1999) Phase I and pharmacokinetic study of temozolomide on a daily-for-5-days schedule in patients with advanced solid malignancies. J Clin Oncol 17:2604鈥?613PubMed
  22.Barazzuol L, Jena R, Burnet NG, Jeynes JC, Merchant MJ, Kirkby KJ, Kirkby NF (2012) In vitro evaluation of combined temozolomide and radiotherapy using X rays and high-linear energy transfer radiation for glioblastoma. Radiat Res 177:651鈥?62PubMed CrossRef
  23.Brunet JP, Tamayo P, Golub TR, Mesirov JP (2004) Metagenes and molecular pattern discovery using matrix factorization. Proc Natl Acad Sci USA 101:4164鈥?169. doi:10.鈥?073/鈥媝nas.鈥?308531101 PubMedCentral PubMed CrossRef
  24.Wu G, Stein L (2012) A network module-based method for identifying cancer prognostic signatures. Genome Biol 13:R112. doi:10.鈥?186/鈥媑b-2012-13-12-r112 PubMedCentral PubMed CrossRef
  25.Wu G, Feng X, Stein L (2010) A human functional protein interaction network and its application to cancer data analysis. Genome Biol 11:R53. doi:10.鈥?186/鈥媑b-2010-11-5-r53 PubMedCentral PubMed CrossRef
  26.Notta F, Mullighan CG, Wang JC, Poeppl A, Doulatov S, Phillips LA, Ma J, Minden MD, Downing JR, Dick JE (2011) Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 469:362鈥?67. doi:10.鈥?038/鈥媙ature09733 PubMed CrossRef
  27.Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267鈥?84. doi:10.鈥?146/鈥媋nnurev.鈥媘ed.鈥?8.鈥?62105.鈥?04854 PubMed CrossRef
  28.Barami K, Fernandes R (2012) Incidence, risk factors and management of delayed wound dehiscence after craniotomy for tumor resection. J Clin Neurosci 19:854鈥?57. doi:10.鈥?016/鈥媕.鈥媕ocn.鈥?011.鈥?9.鈥?25 PubMed CrossRef
  29.Chang SM, Parney IF, McDermott M, Barker FG 2nd, Schmidt MH, Huang W, Laws ER Jr, Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M, Glioma Outcomes I (2003) Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg 98:1175鈥?181. doi:10.鈥?171/鈥媕ns.鈥?003.鈥?8.鈥?.鈥?175 PubMed CrossRef
  30.Facchino S, Abdouh M, Chatoo W, Bernier G (2010) BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 30:10096鈥?0111. doi:10.鈥?523/鈥婮NEUROSCI.鈥?634-10.鈥?010 PubMed CrossRef
  31.Tandle AT, Kramp T, Kil WJ, Halthore A, Gehlhaus K, Shankavaram U, Tofilon PJ, Caplen NJ, Camphausen K (2013) Inhibition of polo-like kinase 1 in glioblastoma multiforme induces mitotic catastrophe and enhances radiosensitisation. Eur J Cancer 49:3020鈥?028. doi:10.鈥?016/鈥媕.鈥媏jca.鈥?013.鈥?5.鈥?13 PubMedCentral PubMed CrossRef
  32.Lee C, Fotovati A, Triscott J, Chen J, Venugopal C, Singhal A, Dunham C, Kerr JM, Verreault M, Yip S, Wakimoto H, Jones C, Jayanthan A, Narendran A, Singh SK, Dunn SE (2012) Polo-like kinase 1 inhibition kills glioblastoma multiforme brain tumor cells in part through loss of SOX2 and delays tumor progression in mice. Stem Cells 30:1064鈥?075. doi:10.鈥?002/鈥媠tem.鈥?081 PubMed CrossRef
  
• 作者单位：Maleeha A. Qazi (1) (2)
  Parvez Vora (1) (3)
  Chitra Venugopal (1) (3)
  Nicole McFarlane (1) (3)
  Minomi K. Subapanditha (1) (2)
  Naresh K. Murty (3)
  John A. Hassell (2) (4)
  Robin M. Hallett (2) (4)
  Sheila K. Singh (1) (2) (3)
  
  1. McMaster Stem Cell and Cancer Research Institute, McMaster University, MDCL 5027, 1200 Main Street West, Hamilton, ON, L8S 4K1, Canada
  2. Department of Biochemistry and Biomedical Sciences, Faculty of Health Sciences, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4L8, Canada
  3. Department of Surgery, Faculty of Health Sciences, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4L8, Canada
  4. McMaster Centre for Functional Genomics, McMaster University, 1200 Main Street West, Hamilton, ON, L8N 3Z5, Canada
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Oncology
  
• 出版者：Springer Netherlands
• ISSN：1573-7373

文摘

Glioblastoma (GBM) is the most common and aggressive primary brain tumor in adults with average disease relapse at 9 months and median survival rarely extending beyond 15 months. Brain tumor stem cells (BTSCs) have been implicated in not only initiating GBM but also conferring resistance to therapy. However, it is not clear whether the BTSC population that initiates tumor growth is also responsible for GBM recurrence. In this study, we have developed a novel in vitro treatment model to profile the evolution of primary treatment-na茂ve GBM BTSCs through chemoradiotherapy. We report that our in vitro model enriched for a CD15+/CD133鈭?BTSC population, mirroring the phenotype of BTSCs in recurrent GBM. We also show that in vitro treatment increased stem cell gene expression as well as self-renewal capacity of primary GBMs. In addition, the chemoradiotherapy-refractory gene signature obtained from gene expression profiling identified a hyper-aggressive subtype of glioma. The delivery of in vitro chemoradiotherapy to primary GBM BTSCs models several aspects of recurrent GBM biology, and could be used as a discovery and drug-screening platform to uncover new biological drivers and therapeutic targets in GBM. Keywords GBM Brain tumor stem cell Chemotherapy Radiotherapy CD15 CD133