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Volume = 46,=20 Number 4 (10/2009)

(page : 385-8)

Clinical Article

Methylation Status of the=20 O6-Methylguanine-Deoxyribonucleic Acid = Methyltransferase Gene=20 Promoter in World Health Organization Grade III = Gliomas=20
Seung-Heon Yang, MD1;Yong Hwy Kim, = MD1;Jin Wook=20 Kim, MD1;Chul-Kee Park, MD, PhD1;Sung-Hye Park, MD2; = and=20 Hee-Won Jung, MD1;
1;Departments of=20 Neurosurgery, and 2;Pathology, Seoul National = University=20 College of Medicine, Seoul, Korea=20

Objective : We=20 analyzed the methylation status of the = O6-methylguanine-DNA=20 methyltransferase (MGMT) gene promoter in World Health = Organization (WHO) grade III gliomas in association = with other=20 molecular markers to evaluate their=20 prevalence.

Methods : The samples = of a=20 total of 36 newly WHO grade III glioma patients = including 19=20 anaplastic oligodendrogliomas (AO), 7 anaplastic=20 oligoastrocytomas (AOA), and 10 anaplastic = astrocytomas (AA)=20 were analyzed. The methylation status of the MGMT gene = promoter was confirmed by methylation-specific = polymerase=20 chain reaction. The 1p/19q chromosomal deletion status = and=20 EGFR amplification were assessed by Fluorescence=20 In-Situ Hybridization. MGMT, EGFR, EGFRvIII, = and p53=20 expression were analyzed by immunohistochemical=20 staining.

Results : The MGMT gene = promoter=20 was methylated in 32 (88.9%) and unmethylated in 4 = (11.2%).=20 Among them, all of the AO and AOA had methylated MGMT = gene=20 promoter without exception. Significant associations = between=20 MGMT gene promoter hypermethylation and 1p/19q = deletion was=20 observed (p =3D 0.003). Other molecular markers = failed to=20 show significant associations between MGMT gene = promoter=20 statuses.

Conclusion : There was = extensive=20 epigenetic silencing of MGMT gene in high grade = gliomas with=20 oligodendroglial component. Together with frequent = 1p/19q=20 co-deletion in oligodendroglial tumors, this may add = plausible=20 explanations supporting the relative favorable = prognosis in=20 oligodendroglial tumors compared with pure astrocytic=20 tumors.

Key=20 words:MGMT gene=20 = promoter;Methylation;1p/19q;Oligodendroglioma;Methylation-specific=20 PCR.

Address for=20 reprints : Chul-Kee Park, M.D., Ph.D., Department = of=20 Neurosurgery, Seoul National University College of=20 Medicine,101 Daehak-ro, Jongno-gu, Seoul 110-799,=20 Korea
Tel : +82-2-2072-0347, Fax : = +82-2-741-8594,=20 E-mail : mailto:nsckpark@paran.com

<= /FONT>

INTRODUCTION

   Anaplastic = astrocytoma=20 (AA), anaplastic oligodendroglioma (AO), and = anaplastic=20 oligoastrocytoma (AOA) are classified into the = histological=20 categories of World Health Organization (WHO) grade = III=20 gliomas, even though their classification based on the = known=20 molecular biology information remains controversial8,9,12,17).=20 O6-methylguanine- DNA methyltransferase (MGMT) is an = enzyme in=20 the DNA repair process that specifically removes = cytotoxic O6-=20 alkylguanine adducts, thus mediating resistance to = alkylating=20 agents16).=20 The role of this DNA repair enzyme in glioblastoma, = that=20 protects the tumor cells against alkylating and = methylating=20 chemotherapeutic agents, resulting in drug resistance = is well=20 studied18).=20 MGMT methylation prevalence in glioblastoma was = reported to be=20 from 30% to 50%2,6,15).=20 However, the investigation for the prevalence of MGMT = gene=20 promoter methylation status as well as their clinical=20 implication in WHO grade III glioma is sparse. = Therefore, we=20 evaluated the methylation status of the MGMT gene = promoter in=20 WHO grade III gliomas using the methylation-specific=20 polymerase chain reaction (MSP)=20 method.

MATERIALS AND = METHODS

Study=20 population
   A total of 36 = newly=20 diagnosed World Health Organization (WHO) grade III = glioma=20 patients were included in this study. Histological = diagnosis=20 according to the WHO 2007 classification was assorted = AO in 19=20 patients, AOA in 7 patients and anaplastic astrocytoma = (AA) in=20 10 patients. The study population consisted of 18 men = and 18=20 women ranging in age from 20 to 79 years (mean, 46.6 = years).=20 All patients underwent surgical removal or biopsy = sampling of=20 their tumor. And, the adjuvant conventional = radiotherapy and=20 chemotherapy were performed after pathologic diagnosis = in all=20 patients.

Methylation-specific = polymerase=20 chain reaction
   The methylation = status of=20 the MGMT gene promoter was confirmed by MSP. Tissue = was=20 dissected from paraffin blocks and put into = polyethylene=20 microtubes. After deparaffinization with xylene and = alcohol,=20 the blocks were dissolved in a lysis buffer solution=20 containing proteinase K. For the MSP, purified DNA was = modified by sodium bisulfite treatment using an EZ DNA = methylation-Gold Kit(tm) (Catalog No. D5005; Zymo = Research,=20 Orange, CA, USA). The primer sequences for the MGMT = were as=20 follows : methylated forward : 5 TTT CGA CGT TCG TAG = GTT TTC=20 GC 3 methylated reverse : 5 GCA CTC TTC CGA AAA CGA = AAC G 3 ,=20 unmethylated forward : 5 TTT GTG TTT TGA TGT TTG TAG = GTT TTT=20 GT 3 , unmethylated reverse : 5 AAC TCC ACA CTC TTC = CAA AAA=20 CAA AAC A 3 . The annealing temperature was 64=A1=C9. = The PCR=20 products obtained were electrophoresed in 2% agarose = gels and=20 visualized under ultraviolet illumination after = staining with=20 ethidium bromide. CpGenome universal unmethylated = (Catalog No.=20 S7822; Chemicon, Temecula, CA, USA) and methylated DNA = sets=20 (Catalog No. S 7821; Chemicon) were used as negative = and=20 positive controls respectively.
   For = the=20 evaluation of the assay results, the products from the = controls were examined first. The MGMT gene promoter = fragments=20 in the controls should be observed at 80 and 92 base = pairs in=20 the methylated DNA-methylated primer and unmethylated=20 DNA-unmethylated primer combinations respectively. The = methylated DNA-unmethylated primer and unmethylated=20 DNA-methylated primer controls should not show any = bands. If=20 the control results were acceptable, patient samples = were=20 evaluated for the presence of amplification with the=20 methylated and unmethylated primers. The results were=20 interpreted as positive if MGMT gene promoter = methylation was=20 detected as a fragment of 80 base pairs observed on = the gel,=20 and negative if MGMT gene promoter methylation was not = detected with the methylated primers.

Fluorescence = in-situ=20 hybridization
   The 1p/19q = chromosomal=20 deletion status and epidermal growth factor receptor = (EGFR)=20 amplification were assessed by rluorescence = in-situ=20 hybridization (FISH) on paraffin sections obtained = during=20 surgery. The procedure and materials are followed as=20 previously described7).

Immunohistoche= mistry
  =20 MGMT, EGFR, epidermal growth factor receptor = variant III=20 (EGFRvIII), and p53 expression were analyzed by=20 immunohistochemical staining. Immunohistochemical = staining was=20 done using the conventional labeled streptavidin-=20 biotin-peroxidase method (LSAB Kit, DAKO, Glostrup, = Denmark)=20 according to the manufacturer's protocol. The used = antibodies=20 are as follows; MGMT (Neomarkers, Fermont, CA, USA), = EGFR=20 (Zymed, San Francisco, CA, USA), EGFRvIII (DAKO, = Glostrup,=20 Denmark), and p53 (DAKO, Glostrup, Denmark).=20 Immunohistochemistry results were semiquantitatively = graded as=20 < 5% (negative), 5-10% (1+), or >10% (2+), based = on the=20 percentage of tumor cells showing immunoreactivity. We = considered more than 1+ as positive for corresponding=20 markers.

Statistical = analysis
  =20 For analyzing associations between markers, the = chisquare=20 test was used for parametric comparisons. Statistical=20 significance was accepted at probability values of = less than=20 0.05. These statistical analyses were performed with = the aid=20 of SPSS software (version 12.0; SPSS Inc., Chicago, = IL,=20 USA).

RESULTS

Methylation status of the MGMT gene = promoter and=20 MGMT expression
   Of the 36 patients = whose=20 samples were analyzed, the MGMT gene promoter was = methylated=20 in 32 (88.9%) and unmethylated in 4 (11.2%). The = results=20 according to the histological classification is = summarized in=20 Table=20 1. Interestingly, all the high grade = gliomas with=20 oligodendroglial component (AO or AOA) had methylated = MGMT=20 gene promoter. Comparison with the = immunohistochemistry result=20 revealed that 81.5% of the analyzable samples showed = matched=20 results which include methylated MGMT gene promoter = and=20 negative MGMT gene promoter expression or vice=20 versa.

Relationships between MGMT gene = promoter=20 status and other molecular = markers
  =20 Associations between the MGMT gene promoter = methylation=20 status and other molecular markers such as 1p/19q = deletion,=20 EGFR amplification, EGFR expression, EGFRvIII = expression and=20 p53 expression are summarized in Table=20 2. Of 19 patients with AOs, 1p/19q = co-deletion was=20 observed in 18 patients. And, 3 of 7 patients with AOA = revealed intact 1p/19q while the others had deletion = in either=20 1p or 19q. All patients with AA had intact 1p/19q = chromosome=20 except for 2 patients who showed deletion in 1p and in = 19q,=20 respectively. Significant associations between MGMT = gene=20 promoter hypermethylation and 1p/19q deletion was = observed=20 (p =3D 0.003) which implies strong evidence of = MGMT gene=20 promoter hypermethylation in high grade = oligodendroglial=20 tumors. EGFR amplification was not observed in any of = the=20 present series of samples and other molecular markers = failed=20 to show significant associations between MGMT gene = promoter=20 statuses.

Relationships between EGFR=20 amplification by FISH and expression of EGFR or = EGFRvIII on=20 immunohistochemical staining
   = EGFR=20 amplification was assessed by FISH in 32 available = samples and=20 the results were negative for all cases. Of 32 = samples,=20 immunohistochemical staining was done in 30 with EGFR = and 17=20 with EGFRvIII. Positive immumoreactivity was observed = with=20 EGFR in 14 (46.7%) samples and with EGFRvIII in 13=20 (76.5%).

DISCUSSION

   The present study clearly = showed that=20 high grade oligodendroglial tumors are always = hypermethylated=20 in the MGMT gene promoter. Only a few studies reported = the=20 status of MGMT gene promoter methylation in gliomas = other than=20 glioblastoma. Mollemann et al.13)=20 reported that MGMT hypermethylation and low or absent=20 expression are frequent in oligodendroglial tumors = that 46 of=20 52 tumors (88%) showed MGMT gene promoter = hypermethylation.=20 Among their 23 AOs and 11 AOAs, the MGMT gene promoter = was not=20 methylated in only 1 and 2 samples respectively and = those=20 samples showed no 1p/19q co-deletion13).=20 Dong et al.3)=20 reported that the prevalence on MGMT gene promoter=20 hypermethylation detected by MSP analysis was 60% of = 43=20 oligodendroglial tumors including 67% of 15 AO/AOAs. = Their=20 data showed significant association between = hypermethylation=20 of MGMT gene promoter and 1p/19q codeletion3).=20 Alonso et al.1)=20 also reported that as much as 80% of 41 = oligodendroglial tumor=20 samples were hypermethylated in their MGMT gene = promoter and=20 among them, 85% of 13 AOs were hypermethylated. = Contrast to=20 the high frequency of methylation rate of MGMT gene = promoter=20 in AO/AOAs, that of AA was found to be relatively low = that=20 less than 50% were methylated according to the = previous=20 studies4,5).=20 Taken together with the previous and the present = study,=20 transcriptional silencing of the MGMT gene by = hypermethylation=20 in oligodendroglial tumor especially in high grade may = contribute to the tumor's sensitivity to chemotherapy. = Nutt et=20 al.14)=20 showed that the low activity of MGMT is sufficient to = account=20 for increased sensitivity of oligodendrocytic cells to = chemotherapeutic drugs.
   There = are=20 evidences that the MGMT gene promoter methylation is=20 associated with tumor progression in oligodendroglial = tumors.=20 The presence of hypermethylation of MGMT in WHO grade = II=20 astrocytoma/oligodendroglioma is only 31%5).=20 Lavon et al.11)=20 performed a longitudinal assessment of epigenetic = aberrant=20 MGMT gene promoter methylation with 46 paired early = and=20 progressive oligodendrogliomas from 23 patients, and=20 correlated them with tumor phenotype in a series of=20 progressive oligodendroglial tumors. They demonstrated = that=20 the MGMT gene promoter methylation is more pronounced = at tumor=20 progression, particularly in tumors with an intact 1p = in=20 oligodendroglial tumors and it was postulated that the = MGMT=20 promoter methylation is a late event in progressive=20 oligodendrogliomas11).=20 It is accepted that the oligodendroglial tumor has a = tendency=20 to be methylated in various gene promoters including = MGMT and=20 this may be associated with the initiation and/or = progression=20 of oligodendroglial tumors10).=20 However, whether MGMT gene methylation is an actual = etiologic=20 event for oligodendroglial tumors or only a prognostic = factor=20 needs further investigation10).

CONCLUSION

   = Our study for MGMT gene=20 promoter methylation status in 36 WHO grade III = gliomas=20 revealed extensive epigenetic silencing of MGMT gene = in high=20 grade gliomas with oligodendroglial component. = Together with=20 frequent 1p/19q co-deletion in oligodendroglial = tumors, this=20 may add plausible explanations supporting the relative = favorable prognosis in oligodendroglial tumors = compared with=20 pure astrocytic=20 = tumors.

REFERENCES:

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