Top

Published in:

01-07-2005 | Regular Paper

Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors

Authors: Se Hoon Kim, Hoguen Kim, Tai Seung Kim

Published in: Acta Neuropathologica | Issue 1/2005

Abstract

To identify a better diagnostic criteria for oligodendroglial tumors, we investigated the clinical, histological, and immunohistochemical features that would be able to predict a 1p/19q loss of heterozygosity (LOH) in these tumors. We performed a PCR-based LOH test with the 1p and 19q microsatellite markers by microdissecting tumor in 56 samples (44 oligodendrogliomas and 12 mixed oligoastrocytomas) of paraffin-embedded tissue. Patients with oligodendroglial tumors with 1p/19q LOH had a statistically significant better prognosis for overall survival. Comparative analysis of several features indicated that the 1p/19q LOH tumors were associated with two histological features, “tumor cellularity” and “perinuclear halo,” and low O⁶-methylguanine-DNA-methyltransferase (MGMT) expression and high cytoplasmic glutathione S-transferase pi (GST-π) expression. In addition, the incidence of 1p/19q LOH was infrequent in the youngest age category (less than 20 years old) studied. Using the new features, we could predict the 1p/19q status of oligodendroglial tumors with greater than 90% accuracy. Therefore, applying these features in clinical practice, would be helpful in clarifying oligodendroglial tumor diagnosis.

Ali-Osman F, Brunner JM, Kutluk TM, Hess K (1997) Prognostic significance of glutathione S-transferase pi expression and subcellular localization in human gliomas. Clin Cancer Res 3:2253–2261PubMed

Alonso ME, Bello MJ, Gonzalez-Gomez P, Arjona D, Lomas J, Campos JM de, Isla A, Sarasa JL, Rey JA (2003) Aberrant promoter methylation of multiple genes in oligodendrogliomas and ependymomas. Cancer Genet Cytogenet 144:134–142CrossRefPubMed

Bauman GS, Ino Y, Ueki K, Zlatescu MC, Fisher BJ, Macdonald DR, Stitt L, Louis DN, Cairncross JG (2000) Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 48:825–830CrossRefPubMed

Buccoliero AM, Caldarella A, Arganini L, Mennonna P, Ammanati F, Taddei A, Taddei GL (2003) Oligodendroglioma: CD44 as a possible prognostic opportunity. Clin Neuropathol 22:169–175PubMed

Burger PC, Minn AY, Smith JS, Borell TJ, Jedlicka AE, Huntley BK, Goldthwaite PT, Jenkins RB, Feuerstein BG (2001) Losses of chromosomal arms 1p and 19q in the diagnosis of oligodendroglioma. A study of paraffin-embedded sections. Mod Pathol 14:842–853CrossRefPubMed

Cairncross JG, Macdonald DR (1988) Successful chemotherapy for recurrent malignant oligodendroglioma. Ann Neurol 23:360–364CrossRefPubMed

Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, Hammond RR, Silver JS, Stark PC, Macdonald DR, Ino Y, Ramsay DA, Louis DN (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst 90:1473–1479PubMed

Coons SW, Johnson PC, Scheithauer BW, Yates AJ, Pearl DK (1997) Improving diagnostic accuracy and interobserver concordance in the classification and grading of primary gliomas. Cancer 79:1381–1393CrossRefPubMed

Dong SM, Pang JC, Poon WS, Hu J, To KF, Chang AR, Ng HK (2001) Concurrent hypermethylation of multiple genes is associated with grade of oligodendroglial tumors. J Neuropathol Exp Neurol 60:808–816PubMed

10.

Fallon KB, Palmer CA, Roth KA, Nabors LB, Wang W, Carpenter M, Banerjee R, Forsyth P, Rich K, Perry A (2004) Prognostic value of 1p, 19q, 9p, 10q, and EGFR-FISH analyses in recurrent oligodendrogliomas. J Neuropathol Exp Neurol 63:314–322PubMed

11.

Hoang-Xuan K, He J, Huguet S, Mokhtari K, Marie Y, Kujas M, Leuraud P, Capelle L, Delattre JY, Poirier J, Broet P, Sanson M (2001) Molecular heterogeneity of oligodendrogliomas suggests alternative pathways in tumor progression. Neurology 57:1278–1281PubMed

12.

Hongeng S, Brent TP, Sanford RA, Li H, Kun LE, Heideman RL (1997) O⁶-Methylguanine-DNA methyltransferase protein levels in pediatric brain tumors. Clin Cancer Res 3:2459–2463PubMed

13.

Ino Y, Betensky RA, Zlatescu MC, Sasaki H, Macdonald DR, Stemmer-Rachamimov AO, Ramsay DA, Cairncross JG, Louis DN (2001) Molecular subtypes of anaplastic oligodendroglioma: implications for patient management at diagnosis. Clin Cancer Res 7:839–845PubMed

14.

Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, Matsumoto T, Tamura K, Imai T, Ohnishi T, Fushiki S, Nakamura Y, Yamasaki M, Okano H, Arita N (2001) Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 68:141–152CrossRefPubMed

15.

Kim SH, Kim H, Kim TS (2005) Adequate microsatellite markers for 1p/19q loss of heterozygosity of oligodendroglial tumors in Korean patients. Korean J Pathol 39:22–33

16.

Korshunov A, Golanov A, Sycheva R (2002) Immunohistochemical markers for prognosis of oligodendroglial neoplasms. J Neurooncol 58:237–253CrossRefPubMed

17.

Ligon KL, Alberta JA, Kho AT, Weiss J, Kwaan MR, Nutt CL, Louis DN, Stiles CD, Rowitch DH (2004) The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J Neuropathol Exp Neurol 63:499–509PubMed

18.

Louis DN, Holland EC, Cairncross JG (2001) Glioma classification: a molecular reappraisal. Am J Pathol 159:779–786PubMed

19.

Mollemann M, Wolter M, Felsberg J, Collins VP, Reifenberger G (2005) Frequent promoter hypermethylation and low expression of the MGMT gene in oligodendroglial tumors. Int J Cancer 20:379–385CrossRef

20.

Mueller W, Hartmann C, Hoffmann A, Lanksch W, Kiwit J, Tonn J, Veelken J, Schramm J, Weller M, Wiestler OD, Louis DN, Deimling A von (2002) Genetic signature of oligoastrocytomas correlates with tumor location and denotes distinct molecular subsets. Am J Pathol 161:313–319PubMed

21.

Nutt CL, Noble M, Chambers AF, Cairncross JG (2000) Differential expression of drug resistance genes and chemosensitivity in glial cell lineages correlate with differential response of oligodendrogliomas and astrocytomas to chemotherapy. Cancer Res 60:4812–4818PubMed

22.

Okamoto Y, Di Patre PL, Burkhard C, Horstmann S, Jourde B, Fahey M, Schuler D, Probst-Hensch NM, Yasargil MG, Yonekawa Y, Lutolf UM, Kleihues P, Ohgaki H (2004) Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol 108:49–56CrossRefPubMed

23.

Park SH, Suh YL (2003) Expression of cyclin A and topoisomerase IIalpha of oligodendrogliomas is correlated with tumour grade, MIB-1 labelling index and survival. Histopathology 42:395–402CrossRefPubMed

24.

Perry A (2001) Oligodendroglial neoplasms: current concepts, misconceptions, and folklore. Adv Anat Pathol 8:183–199CrossRefPubMed

25.

Raghavan R, Balani J, Perry A, Margraf L, Vono MB, Cai DX, Wyatt RE, Rushing EJ, Bowers DC, Hynan LS, White CL 3rd (2003) Pediatric oligodendrogliomas: a study of molecular alterations on 1p and 19q using fluorescence in situ hybridization. J Neuropathol Exp Neurol 62:530–537PubMed

26.

Reifenberger G, Louis DN (2003) Oligodendroglioma: toward molecular definitions in diagnostic neuro-oncology. J Neuropathol Exp Neurol 62:111–126PubMed

27.

Reifenberger G, Kros JM, Burger PC, Louis DN, Collins VP (2000) Oligodendroglial tumours. In: Kleihues P, Cavenee WK (eds) Pathology and genetics of tumour of the nervous system, IARC Press, Lyon, pp 55–70

28.

Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP (1994) Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol 145:1175–1190PubMed

29.

Riemenschneider MJ, Koy TH, Reifenberger G (2004) Expression of oligodendrocyte lineage genes in oligodendroglial and astrocytic gliomas. Acta Neuropathol 107:277–282PubMed

30.

Sasaki H, Zlatescu MC, Betensky RA, Johnk LB, Cutone AN, Cairncross JG, Louis DN (2002) Histopathological-molecular genetic correlations in referral pathologist-diagnosed low-grade “oligodendroglioma”. J Neuropathol Exp Neurol 61:58–63PubMed

31.

Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, Hosek SM, Kimmel D, Yates A, Burger PC, Scheithauer BW, Jenkins RB (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645PubMed

32.

Tanaka S, Kamitani H, Amin MR, Watanabe T, Oka H, Fujii K, Nagashima T, Hori T (2000) Preliminary individual adjuvant therapy for gliomas based on the results of molecular biological analyses for drug-resistance genes. J Neurooncol 46:157–171CrossRefPubMed

33.

Thiessen B, Maguire JA, McNeil K, Huntsman D, Martin MA, Horsman D (2003) Loss of heterozygosity for loci on chromosome arms 1p and 10q in oligodendroglial tumors: relationship to outcome and chemosensitivity. J Neurooncol 64:271–278CrossRefPubMed

34.

Ueki K, Nishikawa R, Nakazato Y, Hirose T, Hirato J, Funada N, Fujimaki T, Hojo S, Kubo O, Ide T, Usui M, Ochiai C, Ito S, Takahashi H, Mukasa A, Asai A, Kirino T (2002) Correlation of histology and molecular genetic analysis of 1p, 19q, 10q, TP53, EGFR, CDK4, and CDKN2A in 91 astrocytic and oligodendroglial tumors. Clin Cancer Res 8:196–201PubMed

35.

Van den Bent MJ, Looijenga LH, Langenberg K, Dinjens W, Graveland W, Uytdewilligen L, Sillevis Smitt PA, Jenkins RB, Kros JM (2003) Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features. Cancer 97:1276–1284CrossRefPubMed

36.

Watanabe T, Nakamura M, Kros JM, Burkhard C, Yonekawa Y, Kleihues P, Ohgaki H (2002) Phenotype versus genotype correlation in oligodendrogliomas and low-grade diffuse astrocytomas. Acta Neuropathol 103:267–275CrossRefPubMed

37.

Yokoo H, Nobusawa S, Takebayashi H, Ikenaka K, Isoda K, Kamiya M, Sasaki A, Hirato J, Nakazato Y (2004) Anti-human Olig2 antibody as a useful immunohistochemical marker of normal oligodendrocytes and gliomas. Am J Pathol 164:1717–1725PubMed

38.

Zlatescu MC, TehraniYazdi A, Sasaki H, Megyesi JF, Betensky RA, Louis DN, Cairncross JG (2001) Tumor location and growth pattern correlate with genetic signature in oligodendroglial neoplasms. Cancer Res 61:6713–6715PubMed

Title: Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors
Authors: Se Hoon Kim
Hoguen Kim
Tai Seung Kim
Publication date: 01-07-2005
Publisher: Springer-Verlag
Published in: Acta Neuropathologica / Issue 1/2005
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-005-1020-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Clinical, histological, and immunohistochemical features predicting 1p/19q loss of heterozygosity in oligodendroglial tumors

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2005

Frontotemporal dementia, motor neuron disease and tauopathy: clinical and neuropathological study in a family

α-Synuclein-immunoreactive structure formation is enhanced in sympathetic ganglia of patients with multiple system atrophy

Pediatric embryonal tumor of the cerebellum with rhabdoid cells and novel intracytoplasmic inclusions: distinction from atypical teratoid/rhabdoid tumor

Neuropathological spectrum of cortical dysplasia in children with severe focal epilepsies

Spindle cell oncocytoma of the adenohypophysis: report of two cases

Cerebellopontine calcification: a new entity of idiopathic intracranial calcification?