|
|
|
|
|
|
||
|
|
||||
|
|
||||
|
||||
Pediatric Neuro-Oncology |
Department of Molecular Neuroscience (B.S.-M., T.R., T.J.W.) and Division of Neurosurgery (D.G.T.T.), Institute of Neurology, National Hospital for Neurology and Neurosurgery, and Department of Molecular Haematology, Institute of Child Health (M.H.), University College London, London; Department of Neurosurgery, Great Ormond Street Hospital for Sick Children NHS Trust, London (W.H., R.H., D.T.); Research Institute in Healthcare Science, University of Wolverhampton, Wolverhampton (J.L.D.); UK
3 Address correspondence to Tracy J. Warr, Department of Molecular Neuroscience, Neuro-Oncology Group, Institute of Neurology, Queen Square, London WC1N 3BG, UK (T.Warr{at}ion.ucl.ac.uk).
Abstract
Ependymomas are glial cell-derived tumors characterized by varying degrees of chromosomal abnormalities and variability in clinical behavior. Cytogenetic analy-sis of pediatric ependymoma has failed to identify consistent patterns of abnormalities, with the exception of monosomy of 22 or structural abnormalities of 22q. In this study, a total of 19 pediatric ependymoma samples were used in a series of expression profiling, quantitative real-time PCR (Q-PCR), and loss of heterozygosity experiments to identify candidate genes involved in the development of this type of pediatric malignancy. Of the 12,627 genes analyzed, a subset of 112 genes emerged as being abnormally expressed when compared to three normal brain controls. Genes with increased expression included the oncogene WNT5A; the p53 homologue p63; and several cell cycle, cell adhesion, and proliferation genes. Underexpressed genes comprised the NF2 interact-ing gene SCHIP-1 and the adenomatous polyposis coli (APC)-associated gene EB1 among others. We validated the abnormal expression of six of these genes by Q-PCR. The subset of differentially expressed genes also included four underexpressed transcripts mapping to 22q12.3-13.3. By Q-PCR we show that one of these genes, CBX7 (22q13.1), was deleted in 55% of cases. Other genes mapping to cytogenetic hot spots included two overexpressed and three underexpressed genes mapping to 1q31-41 and 6q21-q24.3, respectively. These genes represent candidate genes involved in ependymoma tumorigenesis. To the authors' knowledge, this is the first time microarray analysis and Q-PCR have been linked to identify heterozygous/homozygous deletions.
References
Affymetrix (2004) GeneChip Expression Analysis Technical Manual. Affymetrix, Santa Clara, Calif.
Almeida, A., Zhu, X.X., Vogt, N., Tyagi, R., Muleris, M., Dutrillaux, A.M., Dutrillaux, B., Ross, D., Malfoy, B., and Hanash, S. (1998) GAC1, a new member of the leucine-rich repeat superfamily on chromosome band 1q32.1, is amplified and overexpressed in malignant gliomas. Oncogene 16,2997 -3002.[CrossRef][ISI][Medline]
Alonso, M.E., Bello, M.J., Arjona, D., Gonzalez-Gomez, P., Lomas, J., de Campos, J.M., Kusak, M.E., Isla, A., and Rey, J.A. (2002) Analysis of the NF2 gene in oligodendrogliomas and ependymomas. Cancer Genet. Cytogenet. 134, 1-5.[CrossRef][Medline]
Alonso, M.E., Bello, M.J., Gonzalez-Gomez, P., Arjona, D., Lomas, J., de Campos, J.M., Isla, A., Sarasa, J.L., and Rey, J.A. (2003) Aberrant promoter methylation of multiple genes in oligodendrogliomas and ependymomas. Cancer Genet. Cytogenet. 144,134 -142.[CrossRef][Medline]
Alonso, M.E., Bello, M.J., Gonzalez-Gomez, P., Arjona, D., de Campos, J.M., Gutierrez, M., and Rey, J.A. (2004) Aberrant CpG island methylation of multiple genes in ependymal tumors. J. Neurooncol. 67,159 -165.[Medline]
Applied Biosystems (1997) User Bulletin #2,Relative Quantitation of Gene Expression . Foster City, Calif.: Applied Biosystems.
Arbeitman, M.N., Furlong, E.E., Imam, F., Johnson, E., Null, B.H.,
Baker, B.S., Krasnow, M.A., Scott, M.P., Davis, R.W., and White, K.P.
(2002) Gene expression during the life cycle of Drosophila
melanogaster. Science
297,2270
-2275.
Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Methodol. 57,289 -300.
Bhattacharjee, M.B., Armstrong, D.D., Vogel, H., and Cooley, L.D. (1997) Cytogenetic analysis of 120 primary pediatric brain tumors and literature review. Cancer Genet. Cytogenet. 97, 39-53.[CrossRef][ISI][Medline]
Biegel, J.A., Zhou, J.Y., Rorke, L.B., Stenstrom, C., Wainwright,
L.M., and Fogelgren, B. (1999) Germ-line and acquired mutations
of INI1 in atyp ical teratoid and rhabdoid tumors. Cancer
Res. 59,74
-79.
Bigner, S.H., McLendon, R.E., Fuchs, H., McKeever, P.E., and Friedman, H.S. (1997) Chromosomal characteristics of childhood brain tumors. Cancer Genet. Cytogenet. 97,125 -134.[CrossRef][ISI][Medline]
Braga, E., Senchenko, V., Bazov, I., Loginov, W., Liu, J., Ermilova, V., Kazubskaya, T., Garkavtseva, R., Mazurenko, N., Kisseljov, F., Lerman, M.I., Klein, G., Kisselev, L., and Zabarovsky, E.R. (2002) Critical tumor-suppressor gene regions on chromosome 3p in major human epithelial malignancies: Allelotyping and quantitative real-time PCR. Int. J. Cancer 100,534 -541.[CrossRef][ISI][Medline]
Brazma, A., Hingamp, P., Quackenbush, J., Sherlock, G., Spellman, P., Stoeckert, C., Aach, J., Ansorge, W., Ball, C.A., Causton, H.C., Gaasterland, T., Glenisson, P., Holstege, F.C.P., Kim, I.F., Markowitz, V., Matese, J.C., Parkinson, H., Robinson, A., Sarkans, U., Schulze-Kremer, S., Stewart, J., Taylor, R., Vilo, J., and Vingron, M. (2001) Minimum information about a microarray experiment (MIAME)—toward standards for microarray data. Nat. Genetics 29,365 -371.[CrossRef][ISI][Medline]
Brehm, A., Miska, E.A., McCance, D.J., Reid, J.L., Bannister, A.J., and Kouzarides, T. (1998) Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391,597 -601.[CrossRef][Medline]
Bryan, E.J., Jokubaitis, V.J., Chamberlain, N.L., Baxter, S.W., Dawson, E., Choong, D.Y., and Campbell, I.G. (2002) Mutation analysis of EP300 in colon, breast and ovarian carcinomas. Int. J. Cancer 102,137 -141.[CrossRef][ISI][Medline]
Carter, M., Nicholson, J., Ross, F., Crolla, J., Allibone, R., Balaji, V., Perry, R., Walker, D., Gilbertson, R., and Ellison, D.W. (2002) Genetic abnormalities detected in ependymomas by comparative genomic hybridisation. Br. J. Cancer 86,929 -939.[CrossRef][ISI][Medline]
Dyer, S., Prebble, E., Davison, V., Davies, P., Ramani, P.,
Ellison, D., and Grundy, R. (2002) Genomic imbalances in
pediatric intracranial ependymomas define clinically relevant groups.
Am. J. Pathol. 161,2133
-2141.
Dyrskjot, L., Thykjaer, T., Kruhoffer, M., Jensen, J.L., Marcussen, N., Hamilton-Dutoit, S., Wolf, H., and Orntoft, T.F. (2003) Identifying distinct classes of bladder carcinoma using microarrays. Nat. Genet. 33,90 -96.[CrossRef][ISI][Medline]
Esteller, M., Silva, J.M., Dominguez, G., Bonilla, F., Matias-Guiu,
X., Lerma, E., Bussaglia, E., Prat, J., Harkes, I.C., Repasky, E.A.,
Gabrielson, E., Schutte, M., Baylin, S.B., and Herman, J.G.
(2000a) Promoter hypermethylation and BRCA1 inactivation in
sporadic breast and ovarian tumors. J. Natl. Cancer
Inst. 92,564
-569.
Esteller, M., Sparks, A., Toyota, M., Sanchez-Cespedes, M.,
Capella, G., Peinado, M.A., Gonzalez, S., Tarafa, G., Sidransky, D., Meltzer,
S.J., Baylin, S.B., and Herman, J.G. (2000b) Analysis of
adenomatous polyposis coli promoter hypermethylation in human cancer.
Cancer Res. 60,4366
-4371.
Gil, J., Bernard, D., Martinez, D., and Beach, D. (2004) Polycomb CBX7 has a unifying role in cellular lifespan. Nat. Cell Biol. 6,67 -72.[CrossRef][ISI][Medline]
Gilbertson, R.J., Bentley, L., Hernan, R., Junttila, T.T., Frank,
A.J., Haapasalo, H., Connelly, M., Wetmore, C., Curran, T., Elenius, K., and
Ellison, D.W. (2002) ERBB receptor signaling promotes ependymoma
cell proliferation and represents a potential novel therapeutic target for
this disease. Clin. Cancer Res.
8,3054
-3064.
Gronwald, J., Storkel, S., Holtgreve-Grez, H., Hadaczek, P.,
Brinkschmidt, C., Jauch, A., Lubinski, J., and Cremer, T. (1997)
Comparison of DNA gains and losses in primary renal clear cell carcinomas and
metastatic sites: Importance of 1q and 3p copy number changes in metastatic
events. Cancer Res. 57,481
-487.
Hartmann, C., Numann, A., Mueller, W., Holtkamp, N., Simon, M., and von Deimling, A. (2004) Fine mapping of chromosome 22q tumor suppressor gene candidate regions in astrocytoma. Int. J. Cancer 108,839 -844.[Medline]
Heideman, R.L. (1979) Tumors of the central nervous system in children. Rocky. Mt. Med. J. 77,27A -32A.[Medline]
Herman, J.G., and Baylin, S.B. (2000) Promoter-region hypermethylation and gene silencing in human cancer. Curr. Top. Microbiol. Immunol. 249,35 -54.[ISI][Medline]
Howng, S.L., Wu, C.H., Cheng, T.S., Sy, W.D., Lin, P.C., Wang, C., and Hong, Y.R. (2002) Differential expression of Wnt genes, beta-catenin and E-cadherin in human brain tumors. Cancer Lett. 183,95 -101.[Medline]
Ino, Y., Silver, J.S., Blazejewski, L., Nishikawa, R., Matsutani, M., von Deimling, A., and Louis, D.N. (1999) Common regions of deletion on chromosome 22q12.3-q13.1 and 22q13.2 in human astrocytomas appear related to malignancy grade. J. Neuropathol. Exp. Neurol. 58,881 -885.[ISI][Medline]
Kamiya, M., and Nakazato, Y. (2002) The expression of p73, p21 and MDM2 proteins in gliomas. J. Neurooncol. 59,143 -149.[Medline]
Kleihues, P., Louis, D.N., Scheithauer, B.W., Rorke, L.B., Reifenberger, G., Burger, P.C., and Cavenee, W.K. (2002) The WHO classification of tumors of the nervous system. J. Neuropathol. Exp. Neurol. 61,215 -225.[ISI][Medline]
Korshunov, A., Golanov, A., and Timirgaz, V. (2002) Immunohistochemical markers for prognosis of ependymal neoplasms. J. Neurooncol. 58,255 -270.[CrossRef][Medline]
Korshunov, A., Neben, K., Wrobel, G., Tews, B., Benner, A., Hahn,
M., Golanov, A., and Lichter, P. (2003) Gene expression patterns
in ependymomas correlate with tumor location, grade, and patient age.
Am. J. Pathol. 163,1721
-1727.
Kramer, D.L., Parmiter, A.H., Rorke, L.B., Sutton, L.N., and Biegel, J.A. (1998) Molecular cytogenetic studies of pediatric ependymomas. J. Neurooncol. 37, 25-33.[CrossRef][Medline]
Lewandowicz, G.M., Harding, B., Harkness, W., Hayward, R., Thomas, D.G., and Darling, J.L. (2000) Chemosensitivity in childhood brain tumours in vitro: Evidence of differential sensitivity to lomustine (CCNU) and vincristine. Eur. J. Cancer 36,1955 -1964.
Ljubimova, J.Y., Khazenzon, N.M., Chen, Z., Neyman, Y.I., Turner, L., Riedinger, M.S., and Black, K.L. (2001) Gene expression abnormalities in human glial tumors identified by gene array. Int. J. Oncol. 18,287 -295.[Medline]
Luo, J.H. (2002) Gene expression alterations in human prostate cancer. Drugs Today (Barc.) 38,713 -719.
Mackay, A., Jones, C., Dexter, T., Silva, R.L., Bulmer, K., Jones, A., Simpson, P., Harris, R.A., Jat, P.S., Neville, A.M., Reis, L.F., Lakhani, S.R., and O'Hare, M.J. (2003) cDNA microarray analysis of genes associated with ERBB2 (HER2/neu) overexpression in human mammary luminal epithelial cells. Oncogene 22,2680 -2688.[CrossRef][ISI][Medline]
Magnaghhi-Jaulin, L., Groisman, R., Naguibneva, I., Robin, P., Lorain, S., Le Villain, J.P., Troalen, F., Trouche, D., and Harel-Bellan, A. (1998) Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391,601 -605.[CrossRef][Medline]
Mandel, S., Grunblatt, E., Maor, G., and Youdim, M.B. (2002) Early and late gene changes in MPTP mice model of Parkinson's disease employing cDNA microarray. Neurochem. Res. 27,1231 -1243.[CrossRef][ISI][Medline]
Masaki, T., Shiratori, Y., Rengifo, W., Igarashi, K., Yamagata, M., Kurokohchi, K., Uchida, N., Miyauchi, Y., Yoshiji, H., Watanabe, S., Omata, M., and Kuriyama, S. (2003) Cyclins and cyclin-dependent kinases: Comparative study of hepatocellular carcinoma versus cirrhosis. Hepatology 37,534 -543.[CrossRef][ISI][Medline]
Mazewski, C., Soukup, S., Ballard, E., Gotwals, B., and Lampkin, B. (1999) Karyotype studies in 18 ependymomas with literature review of 107 cases. Cancer Genet. Cytogenet. 113, 1-8.[CrossRef][Medline]
M'soka, T.J., Nishioka, J., Taga, A., Kato, K., Kawasaki, H., Yamada, Y., Yu, A., Komada, Y., and Nobori, T. (2000) Detection of methylthio-adenosine phosphorylase (MTAP) and p16 gene deletion in T cell acute lymphoblastic leukemia by real-time quantitative PCR assay. Leukemia 14,935 -940.[CrossRef][ISI][Medline]
Muleris, M., Almeida, A., Dutrillaux, A.M., Pruchon, E., Vega, F., Delattre, J.Y., Poisson, M., Malfoy, B., and Dutrillaux, B. (1994) Oncogene amplification in human gliomas: A molecular cytogenetic analysis. Oncogene 9,2717 -2722.[ISI][Medline]
Muraoka, M., Konishi, M., Kikuchi-Yanoshita, R., Tanaka, K., Shitara, N., Chong, J.M., Iwama, T., and Miyaki, M. (1996) p300 gene alterations in colorectal and gastric carcinomas. Oncogene 12,1565 -1569.[ISI][Medline]
Nijssen, P.C., Deprez, R.H., Tijssen, C.C., Hagemeijer, A., Arnoldus, E.P., Teepen, J.L., Holl, R., and Niermeyer, M.F. (1994) Familial anaplastic ependymoma: Evidence of loss of chromosome 22 in tumour cells. J. Neurol. Neurosurg. Psychiatry 57,1245 -1248.[Abstract]
Nishida, N., Nishimura, T., Ito, T., Komeda, T., Fukuda, Y., and Nakao, K. (2003) Chromosomal instability and human hepatocarcinogenesis. Histol. Histopathol. 18,897 -909.[ISI][Medline]
Oskam, N.T., Bijleveld, E.H., and Hulsebos, T.J. (2000) A region of common deletion in 22q13.3 in human glioma associated with astrocytoma progression. Int. J. Cancer 85,336 -339.[CrossRef][ISI][Medline]
Paro, R., and Hogness, D.S. (1991) The Polycomb
protein shares a homologous domain with a heterochromatin-associated protein
of Drosophila. Proc. Natl. Acad. Sci. USA
88,263
-267.
Perou, C.M., Sorlie, T., Eisen, M.B., van de Rijn, M., Jeffrey, S.S., Rees, C.A., Pollack, J.R., Ross, D.T., Johnsen, H., Akslen, L.A., Fluge, O., Pergamenschikov, A., Williams, C., Zhu, S.X., Lonning, P.E., Borresen-Dale, A.L., Brown, P.O., and Botstein, D. (2000) Molecular portraits of human breast tumours. Nature 406,747 -752.[CrossRef][Medline]
Petersen, I., Hidalgo, A., Petersen, S., Schluns, K., Schewe, C., Pacyna-Gengelbach, M., Goeze, A., Krebber, B., Knosel, T., Kaufmann, O., Szymas, J., and von Deimling, A. (2000) Chromosomal imbalances in brain metastases of solid tumors. Brain Pathol. 10,395 -401.[Medline]
Pollack, I.F., Gerszten, P.C., Martinez, A.J., Lo, K.H., Shultz, B., Albright, A.L., Janosky, J., and Deutsch, M. (1995) Intracranial ependymomas of childhood: Long-term outcome and prognostic factors. Neurosurgery 37,655 -666.[Medline]
Reardon, D.A., Entrekin, R.E., Sublett, J., Ragsdale, S., Li, H., Boyett, J., Kepner, J.L., and Look, A.T. (1999) Chromosome arm 6q loss is the most common recurrent autosomal alteration detected in primary pediatric ependymoma. Genes Chromosomes Cancer 24,230 -237.[CrossRef][Medline]
Renner, C., Pfitzenmeier, J.P., Gerlach, K., Held, G., Ohnesorge, S., Sahin, U., Bauer, S., and Pfreundschuh, M. (1997) RP1, a new member of the adenomatous polyposis coli-binding EB1-like gene family, is differentially expressed in activated T cells. J. Immunol. 159,1276 -1283.[Abstract]
Rouleau, G.A., Merel, P., Lutchman, M., Sanson, M., Zucman, J., Marineau, C., Hoang-Xuan, K., Demczuk, S., Desmaze, C., Plougastel, B., Pulst, S.M., Lenoir, G., Bijlsma, E., Fashold, R., Dumanski, J., de Jong, P., Parry, D., Eldrige, R., Aurias, A., Delattre, O., and Thomas, G. (1993) Alteration in a new gene encoding a putative membrane-organizing protein causes neurofibromatosis type 2. Nature 363,515 -521.[CrossRef][Medline]
Rubio, M.P., Correa, K.M., Ramesh, V., MacCollin, M.M., Jacoby,
L.B., von Deimling, A., Gusella, J.F., and Louis, D.N. (1994)
Analysis of the neurofibromatosis 2 gene in human ependymomas and
astrocytomas. Cancer Res.
54, 45-47.
Sato, K., Schauble, B., Kleihues, P., and Ohgaki, H. (1996) Infrequent alterations of the p15, p16, CDK4 and cyclin D1 genes in non-astrocytic human brain tumors. Int. J. Cancer 66,305 -308.[CrossRef][Medline]
Schrock, E., Thiel, G., Lozanova, T., du Manoir, S., Meffert, M.C., Jauch, A., Speicher, M.R., Nurnberg, P., Vogel, S., and Janisch, W. (1994) Comparative genomic hybridization of human malignant gliomas reveals multiple amplification sites and nonrandom chromosomal gains and losses. Am. J. Pathol. 144,1203 -1218.[Abstract]
Senchenko, V., Liu, J., Braga, E., Mazurenko, N., Loginov, W., Seryogin, Y., Bazov, I., Protopopov, A., Kisseljov, F.L., Kashuba, V., Lerman, M.I., Klein, G., and Zabarovsky, E.R. (2003) Deletion mapping using quantitative real-time PCR identifies two distinct 3p21.3 regions affected in most cervical carcinomas. Oncogene 22,2984 -2992.[CrossRef][ISI][Medline]
Sevenet, N., Lellouch-Tubiana, A., Schofield, D., Hoang-Xuan, K.,
Gessler, M., Birnbaum, D., Jeanpierre, C., Jouvet, A., and Delattre, O.
(1999) Spectrum of hSNF5/INI1 somatic mutations in human cancer
and genotype-phenotype correlations. Hum. Mol. Genet.
8,2359
-2368.
Slavc, I., MacCollin, M.M., Dunn, M., Jones, S., Sutton, L., Gusella, J.F., and Biegel, J.A. (1995) Exon scanning for mutations of the NF2 gene in pediatric ependymomas, rhabdoid tumors and meningiomas. Int. J. Cancer 64,243 -247.[ISI][Medline]
Suzuki, S.O., and Iwaki, T. (2000) Amplification and overexpression of mdm2 gene in ependymomas. Mod. Pathol. 13,548 -553.[CrossRef][Medline]
Tong, C.Y., Ng, H.K., Pang, J.C., Hui, A.B., Ko, H.C., and Lee, J.C. (1999) Molecular genetic analysis of non-astrocytic gliomas. Histopathology 34,331 -341.[CrossRef][Medline]
Vahteristo, P., Bartkova, J., Eerola, H., Syrjakoski, K., Ojala, S., Kilpivaara, O., Tamminen, A., Kononen, J., Aittomaki, K., Heikkila, P., Holli, K., Blomqvist, C., Bartek, J., Kallioniemi, O.P., and Nevanlinna, H. (2002) A CHEK2 genetic variant contributing to a substantial fraction of familial breast cancer. Am. J. Hum. Genet. 71,432 -438.[CrossRef][ISI][Medline]
van't Veer, L.J., Dai, H., van de Vijver, M.J., He, Y.D., Hart, A.A., Bernards, van't Veer, L.J., Dai, H., van de Vijver, M.J., He, Y.D., Hart, A.A., Bernards, R., and Friend, S.H. (2003) Expression profiling predicts outcome in breast cancer. Breast Cancer Res. 5,57 -58.[ISI][Medline]
Versteege, I., Sevenet, N., Lange, J., Rousseau-Merck, M.F., Ambros, P., Handgretinger, R., Aurias, A., and Delattre, O. (1998) Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394,203 -206.[CrossRef][Medline]
Voehringer, D.W., Hirschberg, D.L., Xiao, J., Lu, Q., Roederer, M.,
Lock, C.B., Herzenberg, L.A., Steinman, L., and Herzenberg, L.A.
(2000) Gene microarray identification of redox and mitochondrial
elements that control resistance or sensitivity to apoptosis. Proc.
Natl. Acad. Sci. USA 97,2680
-2685.
von Haken, M.S., White, E.C., Daneshvar-Shyesther, L., Sih, S., Choi, E., Kalra, R., and Cogen, P.H. (1996) Molecular genetic analysis of chromosome arm 17p and chromosome arm 22q DNA sequences in sporadic pediatric ependymomas. Genes Chromosomes Cancer 17,37 -44.[CrossRef][ISI][Medline]
Wang, H., Wang, H., Shen, W., Huang, H., Hu, L., Ramdas, L., Zhou,
Y.H., Liao, W.S., Fuller, G.N., and Zhang, W. (2003) Insulin-like
growth factor binding protein 2 enhances glioblastoma invasion by activating
invasion-enhancing genes. Cancer Res.
63,4315
-4321.
Ward, S., Harding, B., Wilkins, P., Harkness, W., Hayward, R., Darling, J.L., Thomas, D.G., and Warr, T. (2001) Gain of 1q and loss of 22 are the most common changes detected by comparative genomic hybridisation in paediatric ependymoma. Genes Chromosomes Cancer 32,59 -66.[CrossRef][Medline]
Wasenius, V.M., Hemmer, S., Kettunen, E., Knuutila, S., Franssila,
K., and Joensuu, H. (2003) Hepatocyte growth factor receptor,
matrix metal loproteinase-11, tissue inhibitor of metalloproteinase-1, and
fibronectin are up-regulated in papillary thyroid carcinoma: A cDNA and tissue
microarray study. Clin. Cancer Res.
9, 68-75.
Watson, M.A., Gutmann, D.H., Peterson, K., Chicoine, M.R.,
Kleinschmidt-DeMasters, B.K., Brown, H.G., and Perry, A. (2002)
Molecular charac terization of human meningiomas by gene expression profiling
using high-density oligonucleotide microarrays. Am. J.
Pathol. 161,665
-672.
Zeller, C., Hinzmann, B., Seitz, S., Prokoph, H., Burkhard-Goettges, E., Fischer, J., Jandrig, B., Schwarz, L.E., Rosenthal, A., and Scherneck, S. (2003) SASH1: A candidate tumor suppressor gene on chromosome 6q24.3 is downregulated in breast cancer. Oncogene 22,2972 -2983.[CrossRef][Medline]
Zhao, R., Gish, K., Murphy, M., Yin, Y., Notterman, D., Hoffman,
W.H., Tom, E., Mack, D.H., and Levine, A.J. (2000) Analysis of
p53-regulated gene expression patterns using oligonucleotide arrays.
Genes Dev. 14,981
-993.
This article has been cited by other articles:
|
|
 |
|
  P. Pallante, A. Federico, M. T. Berlingieri, M. Bianco, A. Ferraro, F. Forzati, A. Iaccarino, M. Russo, G. M. Pierantoni, V. Leone, et al. Loss of the CBX7 Gene Expression Correlates with a Highly Malignant Phenotype in Thyroid Cancer Cancer Res., August 15, 2008; 68(16): 6770 - 6778. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Modena, E. Lualdi, F. Facchinetti, J. Veltman, J. F. Reid, S. Minardi, I. Janssen, F. Giangaspero, M. Forni, G. Finocchiaro, et al. Identification of Tumor-Specific Molecular Signatures in Intracranial Ependymoma and Association With Clinical Characteristics J. Clin. Oncol., November 20, 2006; 24(33): 5223 - 5233. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Mendrzyk, A. Korshunov, A. Benner, G. Toedt, S. Pfister, B. Radlwimmer, and P. Lichter Identification of gains on 1q and epidermal growth factor receptor overexpression as independent prognostic markers in intracranial ependymoma. Clin. Cancer Res., April 1, 2006; 12(7): 2070 - 2079. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|
