Article: Protein alterations associated with temozolomide resistance in subclones of human glioblastoma cell lines.

File Download Links for fulltext
(May Require Subscription)
Supplementary
  • Basic View
  • Metadata View
  • XML View
TitleProtein alterations associated with temozolomide resistance in subclones of human glioblastoma cell lines.
AuthorsSun, S2
Wong, TS2
Zhang, XQ2
Pu, JK
Lee, NP2
Day, PJ
Ng, GK
Lui, WM2
Leung, GK
KeywordsChemoresistance
Glioma
Proteomics
Temozolomide
Two-dimensional gel electrophoresis
Issue Date2012
PublisherSpringer Netherlands
CitationJournal Of Neuro-Oncology, 2012, v. 107 n. 1, p. 89-100 [How to Cite?]
DOI: http://dx.doi.org/10.1007/s11060-011-0729-8
AbstractTemozolomide (TMZ) is the standard chemotherapeutic agent for human malignant glioma, but intrinsic or acquired chemoresistance represents a major obstacle to successful treatment of this highly lethal group of tumours. Obtaining better understanding of the molecular mechanisms underlying TMZ resistance in malignant glioma is important for the development of better treatment strategies. We have successfully established a passage control line (D54-C10) and resistant variants (D54-P5 and D54-P10) from the parental TMZ-sensitive malignant glioma cell line D54-C0. The resistant sub-cell lines showed alterations in cell morphology, enhanced cell adhesion, increased migration capacities, and cell cycle arrests. Proteomic analysis identified a set of proteins that showed gradual changes in expression according to their 50% inhibitory concentration (IC(50)). Successful validation was provided by transcript profiling in another malignant glioma cell line U87-MG and its resistant counterparts. Moreover, three of the identified proteins (vimentin, cathepsin D and prolyl 4-hydroxylase, beta polypeptide) were confirmed to be upregulated in high-grade glioma. Our data suggest that acquired TMZ resistance in human malignant glioma is associated with promotion of malignant phenotypes, and our reported molecular candidates may serve not only as markers of chemoresistance but also as potential therapeutic targets in the treatment of TMZ-resistant human malignant glioma, providing a platform for future investigations.
ISSN1573-7373
2011 SCImago Journal Rankings: 0.253
DOIhttp://dx.doi.org/10.1007/s11060-011-0729-8
ISI Accession Number IDWOS:000300313100010
Funding AgencyGrant Number
University of Hong Kong201007176020
Funding Information:

We would like to express our sincere gratitude for the insightful advice and support of Dr. Ching Fai Fung. The work was supported by a small project grant from the University of Hong Kong (project code 201007176020).

PubMed Central IDPMC3273683
ReferencesTate MC, Aghi MK (2009) Biology of angiogenesis and invasion in glioma. Neurotherapeutics 6:447–457. doi: 10.1016/j.nurt.2009.04.001

Norden AD, Wen PY (2006) Glioma therapy in adults. Neurologist 12:279–292. doi: 10.1097/01.nrl.0000250928.26044.47

Mason WP (2008) Emerging drugs for malignant glioma. Expert Opin Emerg Drugs 13:81–94. doi: 10.1517/14728214.13.1.81

Auger N, Thillet J, Wanherdrick K, Idbaih A, Legrier ME, Dutrillaux B, Sanson M, Poupon MF (2006) Genetic alterations associated with acquired temozolomide resistance in SNB-19, a human glioma cell line. Mol Cancer Ther 5:2182–2192. doi: 10.1158/1535-7163.MCT-05-0428

a Fischer J, Costa Carvalho P, da Fonseca CO, Liao L, Degrave WM, a Carvalho M, Yates JR, Domont GB (2011) Chemo-resistant protein expression pattern of glioblastoma cells (A172) to perillyl alcohol. J Proteome Res 10:153–160. doi: 10.1021/pr100677g

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 (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. doi: 10.1056/NEJMoa043330

Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466. doi: 10.1016/S1470-2045(09)70025-7

Dehdashti AR, Hegi ME, Regli L, Pica A, Stupp R (2006) New trends in the medical management of glioblastoma multiforme: the role of temozolomide chemotherapy. Neurosurg Focus 20:E6

Nagasubramanian R, Dolan ME (2003) Temozolomide: realizing the promise and potential. Curr Opin Oncol 15:412–418. doi: 10.1097/00001622-200311000-00002

Friedman HS, Johnson SP, Dong Q, Schold SC, Rasheed BK, Bigner SH, Ali-Osman F, Dolan E, Colvin OM, Houghton P, Germain G, Drummond JT, Keir S, Marcelli S, Bigner DD, Modrich P (1997) Methylator resistance mediated by mismatch repair deficiency in a glioblastoma multiforme xenograft. Cancer Res 57:2933–2936

Bocangel DB, Finkelstein S, Schold SC, Bhakat KK, Mitra S, Kokkinakis DM (2002) Multifaceted resistance of gliomas to temozolomide. Clin Cancer Res 8:2725–2734

Fortin D (2004) The blood-brain barrier should not be underestimated in neuro-oncology. Rev Neurol (Paris) 160:523–532. doi: 10.1016/S0035-3787(04)70981-9

Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW (2005) The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res 65:6394–6400. doi: 10.1158/0008-5472.CAN-05-0715

Oliva CR, Nozell SE, Diers A, McClugage SG 3rd, Sarkaria JN, Markert JM, Darley-Usmar VM, Bailey SM, Gillespie GY, Landar A, Griguer CE (2010) Acquisition of temozolomide chemoresistance in gliomas leads to remodeling of mitochondrial electron transport chain. J Biol Chem 285:39759–39767. doi: 10.1074/jbc.M110.147504

Le Calve B, Rynkowski M, Le Mercier M, Bruyere C, Lonez C, Gras T, Haibe-Kains B, Bontempi G, Decaestecker C, Ruysschaert JM, Kiss R, Lefranc F (2010) Long-term in vitro treatment of human glioblastoma cells with temozolomide increases resistance in vivo through up-regulation of GLUT transporter and aldo-keto reductase enzyme AKR1C expression. Neoplasia 12:727–739

Niclou SP, Fack F, Rajcevic U (2010) Glioma proteomics: status and perspectives. J Proteomics 73:1823–1838. doi: 10.1016/j.jprot.2010.03.007

Jiang R, Mircean C, Shmulevich I, Cogdell D, Jia Y, Tabus I, Aldape K, Sawaya R, Bruner JM, Fuller GN, Zhang W (2006) Pathway alterations during glioma progression revealed by reverse phase protein lysate arrays. Proteomics 6:2964–2971. doi: 10.1002/pmic.200500555

Li J, Zhuang Z, Okamoto H, Vortmeyer AO, Park DM, Furuta M, Lee YS, Oldfield EH, Zeng W, Weil RJ (2006) Proteomic profiling distinguishes astrocytomas and identifies differential tumor markers. Neurology 66:733–736. doi: 10.1212/01.wnl.0000201270.90502.d0

Petrik V, Saadoun S, Loosemore A, Hobbs J, Opstad KS, Sheldon J, Tarelli E, Howe FA, Bell BA, Papadopoulos MC (2008) Serum alpha 2-HS glycoprotein predicts survival in patients with glioblastoma. Clin Chem 54:713–722. doi: 10.1373/clinchem.2007.096792

Schuhmann MU, Zucht HD, Nassimi R, Heine G, Schneekloth CG, Stuerenburg HJ, Selle H (2010) Peptide screening of cerebrospinal fluid in patients with glioblastoma multiforme. Eur J Surg Oncol 36:201–207. doi: 10.1016/j.ejso.2009.07.010

Seyfried NT, Huysentruyt LC, Atwood JA 3rd, Xia Q, Seyfried TN, Orlando R (2008) Up-regulation of NG2 proteoglycan and interferon-induced transmembrane proteins 1 and 3 in mouse astrocytoma: a membrane proteomics approach. Cancer Lett 263:243–252. doi: 10.1016/j.canlet.2008.01.007

Bian XW, Xu JP, Ping YF, Wang Y, Chen JH, Xu CP, Wu YZ, Wu J, Zhou XD, Chen YS, Shi JQ, Wang JM (2008) Unique proteomic features induced by a potential antiglioma agent, Nordy (dl-nordihydroguaiaretic acid), in glioma cells. Proteomics 8:484–494. doi: 10.1002/pmic.200700054

Rajcevic U, Petersen K, Knol JC, Loos M, Bougnaud S, Klychnikov O, Li KW, Pham TV, Wang J, Miletic H, Peng Z, Bjerkvig R, Jimenez CR, Niclou SP (2009) iTRAQ-based proteomics profiling reveals increased metabolic activity and cellular cross-talk in angiogenic compared with invasive glioblastoma phenotype. Mol Cell Proteomics 8:2595–2612. doi: 10.1074/mcp.M900124-MCP200

Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109. doi: 10.1007/s00401-007-0243-4

Luk JM, Lam CT, Siu AF, Lam BY, Ng IO, Hu MY, Che CM, Fan ST (2006) Proteomic profiling of hepatocellular carcinoma in Chinese cohort reveals heat-shock proteins (Hsp27, Hsp70, GRP78) up-regulation and their associated prognostic values. Proteomics 6:1049–1057. doi: 10.1002/pmic.200500306

Sun S, Poon RT, Lee NP, Yeung C, Chan KL, Ng IO, Day PJ, Luk JM (2010) Proteomics of hepatocellular carcinoma: serum vimentin as a surrogate marker for small tumors (< or = 2 cm). J Proteome Res 9:1923–1930. doi: 10.1021/pr901085z

Sun S, Xu MZ, Poon RT, Day PJ, Luk JM (2010) Circulating Lamin B1 (LMNB1) biomarker detects early stages of liver cancer in patients. J Proteome Res 9:70–78. doi: 10.1021/pr9002118

Hirose Y, Berger MS, Pieper RO (2001) p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 61:1957–1963

Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797

Maxwell JA, Johnson SP, McLendon RE, Lister DW, Horne KS, Rasheed A, Quinn JA, Ali-Osman F, Friedman AH, Modrich PL, Bigner DD, Friedman HS (2008) Mismatch repair deficiency does not mediate clinical resistance to temozolomide in malignant glioma. Clin Cancer Res 14:4859–4868. doi: 10.1158/1078-0432.CCR-07-4807

Augustine CK, Yoo JS, Potti A, Yoshimoto Y, Zipfel PA, Friedman HS, Nevins JR, Ali-Osman F, Tyler DS (2009) Genomic and molecular profiling predicts response to temozolomide in melanoma. Clin Cancer Res 15:502–510. doi: 10.1158/1078-0432.CCR-08-1916

Hirose Y, Katayama M, Mirzoeva OK, Berger MS, Pieper RO (2005) Akt activation suppresses Chk2-mediated, methylating agent-induced G2 arrest and protects from temozolomide-induced mitotic catastrophe and cellular senescence. Cancer Res 65:4861–4869. doi: 10.1158/0008-5472.CAN-04-2633

Kohmo S, Kijima T, Otani Y, Mori M, Minami T, Takahashi R, Nagatomo I, Takeda Y, Kida H, Goya S, Yoshida M, Kumagai T, Tachibana I, Yokota S, Kawase I (2010) Cell surface tetraspanin CD9 mediates chemoresistance in small cell lung cancer. Cancer Res 70:8025–8035. doi: 10.1158/0008-5472.CAN-10-0996

Hirose Y, Berger MS, Pieper RO (2001) Abrogation of the Chk1-mediated G(2) checkpoint pathway potentiates temozolomide-induced toxicity in a p53-independent manner in human glioblastoma cells. Cancer Res 61:5843–5849

Cazzalini O, Scovassi AI, Savio M, Stivala LA, Prosperi E (2010) Multiple roles of the cell cycle inhibitor p21 (CDKN1A) in the DNA damage response. Mutat Res 704:12–20. doi: 10.1016/j.mrrev.2010.01.009

Chaudhary KS, Abel PD, Stamp GW, Lalani E (2001) Differential expression of cell death regulators in response to thapsigargin and adriamycin in Bcl-2 transfected DU145 prostatic cancer cells. J Pathol 193:522–529. doi: 10.1002/1096-9896(2000)9999:9999%3C::AID-PATH821%3E3.0.CO;2-Y

McInroy L, Maatta A (2007) Down-regulation of vimentin expression inhibits carcinoma cell migration and adhesion. Biochem Biophys Res Commun 360:109–114. doi: 10.1016/j.bbrc.2007.06.036

Trog D, Yeghiazaryan K, Schild HH, Golubnitschaja O (2008) Up-regulation of vimentin expression in low-density malignant glioma cells as immediate and late effects under irradiation and temozolomide treatment. Amino Acids 34:539–545. doi: 10.1007/s00726-007-0007-4

Berchem G, Glondu M, Gleizes M, Brouillet JP, Vignon F, Garcia M, Liaudet-Coopman E (2002) Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 21:5951–5955. doi: 10.1038/sj.onc.1205745

Fukuda ME, Iwadate Y, Machida T, Hiwasa T, Nimura Y, Nagai Y, Takiguchi M, Tanzawa H, Yamaura A, Seki N (2005) Cathepsin D is a potential serum marker for poor prognosis in glioma patients. Cancer Res 65:5190–5194. doi: 10.1158/0008-5472.CAN-04-4134

Sagulenko V, Muth D, Sagulenko E, Paffhausen T, Schwab M, Westermann F (2008) Cathepsin D protects human neuroblastoma cells from doxorubicin-induced cell death. Carcinogenesis 29:1869–1877. doi: 10.1093/carcin/bgn147

Goplen D, Wang J, Enger PO, Tysnes BB, Terzis AJ, Laerum OD, Bjerkvig R (2006) Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 66:9895–9902. doi: 10.1158/0008-5472.CAN-05-4589

Cicchillitti L, Della Corte A, Di Michele M, Donati MB, Rotilio D, Scambia G (2010) Characterisation of a multimeric protein complex associated with ERp57 within the nucleus in paclitaxel-sensitive and -resistant epithelial ovarian cancer cells: the involvement of specific conformational states of beta-actin. Int J Oncol 37:445–454. doi: 10.3892/ijo_00000693

Fu Y, Li J, Lee AS (2007) GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 67:3734–3740. doi: 10.1158/0008-5472.CAN-06-4594

Bulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, Rudolph MG, Burger KN, Honing S (2009) TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185:641–655. doi: 10.1083/jcb.200812042

Hocsak E, Racz B, Szabo A, Mester L, Rapolti E, Pozsgai E, Javor S, Bellyei S, Gallyas F Jr, Sumegi B, Szigeti A (2010) TIP47 protects mitochondrial membrane integrity and inhibits oxidative-stress-induced cell death. FEBS Lett 584:2953–2960. doi: 10.1016/j.febslet.2010.05.027

Hocsak E, Racz B, Szabo A, Pozsgai E, Szigeti A, Szigeti E, Gallyas F Jr, Sumegi B, Javor S, Bellyei S (2010) TIP47 confers resistance to taxol-induced cell death by preventing the nuclear translocation of AIF and endonuclease G. Eur J Cell Biol 89:853–861. doi: 10.1016/j.ejcb.2010.06.010

Heiska L, Carpen O (2005) Src phosphorylates ezrin at tyrosine 477 and induces a phosphospecific association between ezrin and a kelch-repeat protein family member. J Biol Chem 280:10244–10252. doi: 10.1074/jbc.M411353200

Di Cristofano C, Leopizzi M, Miraglia A, Sardella B, Moretti V, Ferrara A, Petrozza V, Della Rocca C (2010) Phosphorylated ezrin is located in the nucleus of the osteosarcoma cell. Mod Pathol 23:1012–1020. doi: 10.1038/modpathol.2010.77

Sun QL, Sha HF, Yang XH, Bao GL, Lu J, Xie YY (2011) Comparative proteomic analysis of paclitaxel sensitive A549 lung adenocarcinoma cell line and its resistant counterpart A549-Taxol. J Cancer Res Clin Oncol 137:521–532. doi: 10.1007/s00432-010-0913-9

Hart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K (2008) Temozolomide for high grade glioma. Cochrane Database Syst Rev (4):CD007415
GrantsIdentification of therapeutic targets to combat glioblastoma drug resistance by proteomic profiling
DC Field
Value
dc.contributor.authorSun, S
dc.contributor.authorWong, TS
dc.contributor.authorZhang, XQ
dc.contributor.authorPu, JK
dc.contributor.authorLee, NP
dc.contributor.authorDay, PJ
dc.contributor.authorNg, GK
dc.contributor.authorLui, WM
dc.contributor.authorLeung, GK
dc.date.accessioned2012-02-21T05:43:33Z
dc.date.available2012-02-21T05:43:33Z
dc.date.issued2012
dc.description.abstractTemozolomide (TMZ) is the standard chemotherapeutic agent for human malignant glioma, but intrinsic or acquired chemoresistance represents a major obstacle to successful treatment of this highly lethal group of tumours. Obtaining better understanding of the molecular mechanisms underlying TMZ resistance in malignant glioma is important for the development of better treatment strategies. We have successfully established a passage control line (D54-C10) and resistant variants (D54-P5 and D54-P10) from the parental TMZ-sensitive malignant glioma cell line D54-C0. The resistant sub-cell lines showed alterations in cell morphology, enhanced cell adhesion, increased migration capacities, and cell cycle arrests. Proteomic analysis identified a set of proteins that showed gradual changes in expression according to their 50% inhibitory concentration (IC(50)). Successful validation was provided by transcript profiling in another malignant glioma cell line U87-MG and its resistant counterparts. Moreover, three of the identified proteins (vimentin, cathepsin D and prolyl 4-hydroxylase, beta polypeptide) were confirmed to be upregulated in high-grade glioma. Our data suggest that acquired TMZ resistance in human malignant glioma is associated with promotion of malignant phenotypes, and our reported molecular candidates may serve not only as markers of chemoresistance but also as potential therapeutic targets in the treatment of TMZ-resistant human malignant glioma, providing a platform for future investigations.
dc.description.grantIdentification of therapeutic targets to combat glioblastoma drug resistance by proteomic profiling
dc.description.grantcode104149
dc.description.naturepublished_or_final_version
dc.description.otherSpringer Open Choice, 21 Feb 2012
dc.identifier.citationJournal Of Neuro-Oncology, 2012, v. 107 n. 1, p. 89-100 [How to Cite?]
DOI: http://dx.doi.org/10.1007/s11060-011-0729-8
dc.identifier.citeulike9884995
dc.identifier.doihttp://dx.doi.org/10.1007/s11060-011-0729-8
dc.identifier.eissn1573-7373
dc.identifier.epage100
dc.identifier.hkuros206154
dc.identifier.isiWOS:000300313100010
Funding AgencyGrant Number
University of Hong Kong201007176020
Funding Information:

We would like to express our sincere gratitude for the insightful advice and support of Dr. Ching Fai Fung. The work was supported by a small project grant from the University of Hong Kong (project code 201007176020).

dc.identifier.issn1573-7373
2011 SCImago Journal Rankings: 0.253
dc.identifier.issue1
dc.identifier.openurl
dc.identifier.pmcidPMC3273683
dc.identifier.pmid21979894
dc.identifier.scopuseid_2-s2.0-84861697239
dc.identifier.spage89
dc.identifier.urihttp://hdl.handle.net/10722/144940
dc.identifier.volume107
dc.languageEng
dc.publisherSpringer Netherlands
dc.relation.ispartofJournal of Neuro-Oncology
dc.relation.referencesTate MC, Aghi MK (2009) Biology of angiogenesis and invasion in glioma. Neurotherapeutics 6:447–457. doi: 10.1016/j.nurt.2009.04.001
dc.relation.referencesNorden AD, Wen PY (2006) Glioma therapy in adults. Neurologist 12:279–292. doi: 10.1097/01.nrl.0000250928.26044.47
dc.relation.referencesMason WP (2008) Emerging drugs for malignant glioma. Expert Opin Emerg Drugs 13:81–94. doi: 10.1517/14728214.13.1.81
dc.relation.referencesAuger N, Thillet J, Wanherdrick K, Idbaih A, Legrier ME, Dutrillaux B, Sanson M, Poupon MF (2006) Genetic alterations associated with acquired temozolomide resistance in SNB-19, a human glioma cell line. Mol Cancer Ther 5:2182–2192. doi: 10.1158/1535-7163.MCT-05-0428
dc.relation.referencesa Fischer J, Costa Carvalho P, da Fonseca CO, Liao L, Degrave WM, a Carvalho M, Yates JR, Domont GB (2011) Chemo-resistant protein expression pattern of glioblastoma cells (A172) to perillyl alcohol. J Proteome Res 10:153–160. doi: 10.1021/pr100677g
dc.relation.referencesStupp 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 (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. doi: 10.1056/NEJMoa043330
dc.relation.referencesStupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459–466. doi: 10.1016/S1470-2045(09)70025-7
dc.relation.referencesDehdashti AR, Hegi ME, Regli L, Pica A, Stupp R (2006) New trends in the medical management of glioblastoma multiforme: the role of temozolomide chemotherapy. Neurosurg Focus 20:E6
dc.relation.referencesNagasubramanian R, Dolan ME (2003) Temozolomide: realizing the promise and potential. Curr Opin Oncol 15:412–418. doi: 10.1097/00001622-200311000-00002
dc.relation.referencesFriedman HS, Johnson SP, Dong Q, Schold SC, Rasheed BK, Bigner SH, Ali-Osman F, Dolan E, Colvin OM, Houghton P, Germain G, Drummond JT, Keir S, Marcelli S, Bigner DD, Modrich P (1997) Methylator resistance mediated by mismatch repair deficiency in a glioblastoma multiforme xenograft. Cancer Res 57:2933–2936
dc.relation.referencesBocangel DB, Finkelstein S, Schold SC, Bhakat KK, Mitra S, Kokkinakis DM (2002) Multifaceted resistance of gliomas to temozolomide. Clin Cancer Res 8:2725–2734
dc.relation.referencesFortin D (2004) The blood-brain barrier should not be underestimated in neuro-oncology. Rev Neurol (Paris) 160:523–532. doi: 10.1016/S0035-3787(04)70981-9
dc.relation.referencesTrivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW (2005) The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res 65:6394–6400. doi: 10.1158/0008-5472.CAN-05-0715
dc.relation.referencesOliva CR, Nozell SE, Diers A, McClugage SG 3rd, Sarkaria JN, Markert JM, Darley-Usmar VM, Bailey SM, Gillespie GY, Landar A, Griguer CE (2010) Acquisition of temozolomide chemoresistance in gliomas leads to remodeling of mitochondrial electron transport chain. J Biol Chem 285:39759–39767. doi: 10.1074/jbc.M110.147504
dc.relation.referencesLe Calve B, Rynkowski M, Le Mercier M, Bruyere C, Lonez C, Gras T, Haibe-Kains B, Bontempi G, Decaestecker C, Ruysschaert JM, Kiss R, Lefranc F (2010) Long-term in vitro treatment of human glioblastoma cells with temozolomide increases resistance in vivo through up-regulation of GLUT transporter and aldo-keto reductase enzyme AKR1C expression. Neoplasia 12:727–739
dc.relation.referencesNiclou SP, Fack F, Rajcevic U (2010) Glioma proteomics: status and perspectives. J Proteomics 73:1823–1838. doi: 10.1016/j.jprot.2010.03.007
dc.relation.referencesJiang R, Mircean C, Shmulevich I, Cogdell D, Jia Y, Tabus I, Aldape K, Sawaya R, Bruner JM, Fuller GN, Zhang W (2006) Pathway alterations during glioma progression revealed by reverse phase protein lysate arrays. Proteomics 6:2964–2971. doi: 10.1002/pmic.200500555
dc.relation.referencesLi J, Zhuang Z, Okamoto H, Vortmeyer AO, Park DM, Furuta M, Lee YS, Oldfield EH, Zeng W, Weil RJ (2006) Proteomic profiling distinguishes astrocytomas and identifies differential tumor markers. Neurology 66:733–736. doi: 10.1212/01.wnl.0000201270.90502.d0
dc.relation.referencesPetrik V, Saadoun S, Loosemore A, Hobbs J, Opstad KS, Sheldon J, Tarelli E, Howe FA, Bell BA, Papadopoulos MC (2008) Serum alpha 2-HS glycoprotein predicts survival in patients with glioblastoma. Clin Chem 54:713–722. doi: 10.1373/clinchem.2007.096792
dc.relation.referencesSchuhmann MU, Zucht HD, Nassimi R, Heine G, Schneekloth CG, Stuerenburg HJ, Selle H (2010) Peptide screening of cerebrospinal fluid in patients with glioblastoma multiforme. Eur J Surg Oncol 36:201–207. doi: 10.1016/j.ejso.2009.07.010
dc.relation.referencesSeyfried NT, Huysentruyt LC, Atwood JA 3rd, Xia Q, Seyfried TN, Orlando R (2008) Up-regulation of NG2 proteoglycan and interferon-induced transmembrane proteins 1 and 3 in mouse astrocytoma: a membrane proteomics approach. Cancer Lett 263:243–252. doi: 10.1016/j.canlet.2008.01.007
dc.relation.referencesBian XW, Xu JP, Ping YF, Wang Y, Chen JH, Xu CP, Wu YZ, Wu J, Zhou XD, Chen YS, Shi JQ, Wang JM (2008) Unique proteomic features induced by a potential antiglioma agent, Nordy (dl-nordihydroguaiaretic acid), in glioma cells. Proteomics 8:484–494. doi: 10.1002/pmic.200700054
dc.relation.referencesRajcevic U, Petersen K, Knol JC, Loos M, Bougnaud S, Klychnikov O, Li KW, Pham TV, Wang J, Miletic H, Peng Z, Bjerkvig R, Jimenez CR, Niclou SP (2009) iTRAQ-based proteomics profiling reveals increased metabolic activity and cellular cross-talk in angiogenic compared with invasive glioblastoma phenotype. Mol Cell Proteomics 8:2595–2612. doi: 10.1074/mcp.M900124-MCP200
dc.relation.referencesLouis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109. doi: 10.1007/s00401-007-0243-4
dc.relation.referencesLuk JM, Lam CT, Siu AF, Lam BY, Ng IO, Hu MY, Che CM, Fan ST (2006) Proteomic profiling of hepatocellular carcinoma in Chinese cohort reveals heat-shock proteins (Hsp27, Hsp70, GRP78) up-regulation and their associated prognostic values. Proteomics 6:1049–1057. doi: 10.1002/pmic.200500306
dc.relation.referencesSun S, Poon RT, Lee NP, Yeung C, Chan KL, Ng IO, Day PJ, Luk JM (2010) Proteomics of hepatocellular carcinoma: serum vimentin as a surrogate marker for small tumors (< or = 2 cm). J Proteome Res 9:1923–1930. doi: 10.1021/pr901085z
dc.relation.referencesSun S, Xu MZ, Poon RT, Day PJ, Luk JM (2010) Circulating Lamin B1 (LMNB1) biomarker detects early stages of liver cancer in patients. J Proteome Res 9:70–78. doi: 10.1021/pr9002118
dc.relation.referencesHirose Y, Berger MS, Pieper RO (2001) p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 61:1957–1963
dc.relation.referencesEsteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797
dc.relation.referencesMaxwell JA, Johnson SP, McLendon RE, Lister DW, Horne KS, Rasheed A, Quinn JA, Ali-Osman F, Friedman AH, Modrich PL, Bigner DD, Friedman HS (2008) Mismatch repair deficiency does not mediate clinical resistance to temozolomide in malignant glioma. Clin Cancer Res 14:4859–4868. doi: 10.1158/1078-0432.CCR-07-4807
dc.relation.referencesAugustine CK, Yoo JS, Potti A, Yoshimoto Y, Zipfel PA, Friedman HS, Nevins JR, Ali-Osman F, Tyler DS (2009) Genomic and molecular profiling predicts response to temozolomide in melanoma. Clin Cancer Res 15:502–510. doi: 10.1158/1078-0432.CCR-08-1916
dc.relation.referencesHirose Y, Katayama M, Mirzoeva OK, Berger MS, Pieper RO (2005) Akt activation suppresses Chk2-mediated, methylating agent-induced G2 arrest and protects from temozolomide-induced mitotic catastrophe and cellular senescence. Cancer Res 65:4861–4869. doi: 10.1158/0008-5472.CAN-04-2633
dc.relation.referencesKohmo S, Kijima T, Otani Y, Mori M, Minami T, Takahashi R, Nagatomo I, Takeda Y, Kida H, Goya S, Yoshida M, Kumagai T, Tachibana I, Yokota S, Kawase I (2010) Cell surface tetraspanin CD9 mediates chemoresistance in small cell lung cancer. Cancer Res 70:8025–8035. doi: 10.1158/0008-5472.CAN-10-0996
dc.relation.referencesHirose Y, Berger MS, Pieper RO (2001) Abrogation of the Chk1-mediated G(2) checkpoint pathway potentiates temozolomide-induced toxicity in a p53-independent manner in human glioblastoma cells. Cancer Res 61:5843–5849
dc.relation.referencesCazzalini O, Scovassi AI, Savio M, Stivala LA, Prosperi E (2010) Multiple roles of the cell cycle inhibitor p21 (CDKN1A) in the DNA damage response. Mutat Res 704:12–20. doi: 10.1016/j.mrrev.2010.01.009
dc.relation.referencesChaudhary KS, Abel PD, Stamp GW, Lalani E (2001) Differential expression of cell death regulators in response to thapsigargin and adriamycin in Bcl-2 transfected DU145 prostatic cancer cells. J Pathol 193:522–529. doi: 10.1002/1096-9896(2000)9999:9999%3C::AID-PATH821%3E3.0.CO;2-Y
dc.relation.referencesMcInroy L, Maatta A (2007) Down-regulation of vimentin expression inhibits carcinoma cell migration and adhesion. Biochem Biophys Res Commun 360:109–114. doi: 10.1016/j.bbrc.2007.06.036
dc.relation.referencesTrog D, Yeghiazaryan K, Schild HH, Golubnitschaja O (2008) Up-regulation of vimentin expression in low-density malignant glioma cells as immediate and late effects under irradiation and temozolomide treatment. Amino Acids 34:539–545. doi: 10.1007/s00726-007-0007-4
dc.relation.referencesBerchem G, Glondu M, Gleizes M, Brouillet JP, Vignon F, Garcia M, Liaudet-Coopman E (2002) Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis. Oncogene 21:5951–5955. doi: 10.1038/sj.onc.1205745
dc.relation.referencesFukuda ME, Iwadate Y, Machida T, Hiwasa T, Nimura Y, Nagai Y, Takiguchi M, Tanzawa H, Yamaura A, Seki N (2005) Cathepsin D is a potential serum marker for poor prognosis in glioma patients. Cancer Res 65:5190–5194. doi: 10.1158/0008-5472.CAN-04-4134
dc.relation.referencesSagulenko V, Muth D, Sagulenko E, Paffhausen T, Schwab M, Westermann F (2008) Cathepsin D protects human neuroblastoma cells from doxorubicin-induced cell death. Carcinogenesis 29:1869–1877. doi: 10.1093/carcin/bgn147
dc.relation.referencesGoplen D, Wang J, Enger PO, Tysnes BB, Terzis AJ, Laerum OD, Bjerkvig R (2006) Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 66:9895–9902. doi: 10.1158/0008-5472.CAN-05-4589
dc.relation.referencesCicchillitti L, Della Corte A, Di Michele M, Donati MB, Rotilio D, Scambia G (2010) Characterisation of a multimeric protein complex associated with ERp57 within the nucleus in paclitaxel-sensitive and -resistant epithelial ovarian cancer cells: the involvement of specific conformational states of beta-actin. Int J Oncol 37:445–454. doi: 10.3892/ijo_00000693
dc.relation.referencesFu Y, Li J, Lee AS (2007) GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 67:3734–3740. doi: 10.1158/0008-5472.CAN-06-4594
dc.relation.referencesBulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, Rudolph MG, Burger KN, Honing S (2009) TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185:641–655. doi: 10.1083/jcb.200812042
dc.relation.referencesHocsak E, Racz B, Szabo A, Mester L, Rapolti E, Pozsgai E, Javor S, Bellyei S, Gallyas F Jr, Sumegi B, Szigeti A (2010) TIP47 protects mitochondrial membrane integrity and inhibits oxidative-stress-induced cell death. FEBS Lett 584:2953–2960. doi: 10.1016/j.febslet.2010.05.027
dc.relation.referencesHocsak E, Racz B, Szabo A, Pozsgai E, Szigeti A, Szigeti E, Gallyas F Jr, Sumegi B, Javor S, Bellyei S (2010) TIP47 confers resistance to taxol-induced cell death by preventing the nuclear translocation of AIF and endonuclease G. Eur J Cell Biol 89:853–861. doi: 10.1016/j.ejcb.2010.06.010
dc.relation.referencesHeiska L, Carpen O (2005) Src phosphorylates ezrin at tyrosine 477 and induces a phosphospecific association between ezrin and a kelch-repeat protein family member. J Biol Chem 280:10244–10252. doi: 10.1074/jbc.M411353200
dc.relation.referencesDi Cristofano C, Leopizzi M, Miraglia A, Sardella B, Moretti V, Ferrara A, Petrozza V, Della Rocca C (2010) Phosphorylated ezrin is located in the nucleus of the osteosarcoma cell. Mod Pathol 23:1012–1020. doi: 10.1038/modpathol.2010.77
dc.relation.referencesSun QL, Sha HF, Yang XH, Bao GL, Lu J, Xie YY (2011) Comparative proteomic analysis of paclitaxel sensitive A549 lung adenocarcinoma cell line and its resistant counterpart A549-Taxol. J Cancer Res Clin Oncol 137:521–532. doi: 10.1007/s00432-010-0913-9
dc.relation.referencesHart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K (2008) Temozolomide for high grade glioma. Cochrane Database Syst Rev (4):CD007415
dc.rightsThe Author(s)
dc.rightsCreative Commons: Attribution 3.0 Hong Kong License
dc.subjectChemoresistance
dc.subjectGlioma
dc.subjectProteomics
dc.subjectTemozolomide
dc.subjectTwo-dimensional gel electrophoresis
dc.titleProtein alterations associated with temozolomide resistance in subclones of human glioblastoma cell lines.
dc.typeArticle
Author Affiliations
  1. University of Manchester
  2. The University of Hong Kong