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Prognostic Significance of the Null Genotype of Glutathione S

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Prognostic Significance of the Null Genotype of Glutathione S Leukemia (2002) 16, 203–208 2002 Nature Publishing Group All rights reserved 0887-6924/02 $25.00 www.nature.com/leu Prognostic significance of the null genotype of glutathione S-transferase-T1 in patients with acute myeloid leukemia: increased early death after chemotherapy T Naoe1, Y Tagawa1, H Kiyoi1, Y Kodera2, S Miyawaki3, N Asou4, K Kuriyama5, S Kusumoto6, C Shimazaki7, K Saito8, H Akiyama9, T Motoji10, M Nishimura11, K Shinagawa12, R Ueda13, H Saito14 and R Ohno15 1Department of Infectious Diseases, Nagoya University School of Medicine, Nagoya, Japan; 2Department of Medicine, Japanese Red Cross Nagoya First Hospital, Nagoya, Japan; 3Department of Medicine, Saiseikai Maebashi Hospital, Maebashi, Japan; 4Second Department of Internal Medicine, Kumamoto University School of Medicine, Kumamoto, Nagasaki, Japan; 5Department of Hematology, Atomic Disease Institute Nagasaki University School of Medicine, Nagasaki, Japan; 6First Department of Internal Medicine, Saitama Medical School, Saitama, Japan; 7Second Department of Medicine, Kyoto Prefectural University of Medicine, Kyoto, Japan; 8Third Department of Internal Medicine, Dokkyo University School of Medicine, Tochigi, Japan; 9Hematology Division, Tokyo Metropolitan Komagome Hospital, Tokyo, Japan; 10Department of Hematology, Tokyo Women’s Medical University, Tokyo, Japan; 11Second Department of Internal Medicine, Chiba University School of Medicine, Chiba, Japan; 12Department of Medicine, Okayama University Medical School, Okayama, Japan; 13Second Department of Internal Medicine, Nagoya City University School of Medicine, Nagoya, Japan; 14Nagoya National Hospital, Nagoya, Japan; and 15Aichi Cancer Center, Nagoya, Japan We investigated the prognostic significance of genetic myeloperoxidase (MPO), the products of which are associated polymorphism in glutathione-S transferase mu 1 (GSTM1), glut- with drug metabolism as well as with detoxication, in de novo athione-S transferase theta 1 (GSTT1), NAD(P)H:quinone oxido- reductase (NQO1) and myeloperoxidase (MPO), the products acute myeloid leukemia (AML). Cytochrome P450 (CYP) 3A4 of which are associated with drug metabolism as well as with is also involved in metabolizing anti-cancer drugs but was detoxication, in 193 patients with de novo acute myeloid leuke- not studied due to lack of polymorphism in the Japanese mia (AML) other than M3. Of the patients, 64.2% were either population.8 homozygous or heterozygous for GSTT1 (GSTT1+), while 35.8% showed homozygous deletions of GSTT1 (GSTT1−). The GSTT1− group had a worse prognosis than the GSTT1+ group (P = 0.04), whereas other genotypes did not affect the outcome. Materials and methods Multivariate analysis revealed that GSTT1− was an independent prognostic factor for overall survival (relative risk: 1.53; P = Patients 0.026) but not for disease-free survival of 140 patients who ach- ieved complete remission (CR). The rate of early death after the − The subjects included 193 patients with previously non- initiation of chemotherapy was higher in the GSTT1 group than treated de novo AML other than M3, who were registered for the GSTT1+ group (within 45 days after initial chemotherapy, P = 0.073; within 120 days, P = 0.028), whereas CR rates and the AML protocols conducted by the Japan Adult Leukemia relapse frequencies were similar. The null genotype of GSTT1 Study Group (JALSG). Twenty-six, 39 and 128 patients were might be associated with increased toxicity after chemo- treated with the AML-87, AML-89 and AML-92 protocols, therapy. respectively.9–11 AML samples were provided through 16 hos- Leukemia (2002) 16, 203–208. DOI: 10.1038/sj/leu/2402361 pitals (about a quarter of JALSG institutes) for the purpose of Keywords: glutathione S-transferase; polymorphism; acute molecular study after informed consent. AML was diagnosed myeloid leukemia; prognosis according to the FAB classification, which was evaluated by a central review committee. Patients whose performance status was 3 or 4 (ECOG classification) were excluded from Introduction the registration. In the AML-87 study,9 induction therapy consisted of daily In acute leukemia, prognosis depends on biological character- behenoyl cytarabine (BHAC) 200 mg/m2, daily 6-mercaptopu- istics including morphology (FAB classification), immuno- rine (6-MP) 70 mg/m2, daily prednisolone (PRD) 40 mg/m2 phenotype, peripheral white blood cell (WBC) counts, and daunorubicin (DNR) 40 mg/m2 on days 1 to 3, and if chromosomal alterations, and many other molecular and necessary on days 7, 8 and 11. The therapy was continued 1–3 phenotypic markers of leukemia cells. Host-sided factors for a 10- to 12-day period until the bone marrow became including the patient’s age and performance status are also severely hypoplastic with less than 5% blasts. In the AML-89 2–5 associated with the prognosis. Genetic polymorphisms study,10 patients were randomized to receive induction ther- have been examined focusing on individual differences in apy that included BHAC (200 mg/m2 by 3 h infusion) or cytar- 6 pharmaco-dynamics, response, and the side-effects of drugs. abine (AraC, 80 mg/m2 by continuous infusion). BHAC or However, it remains to be elucidated whether genetic poly- AraC, and 6-MP 70 mg/m2 were administrated for 10 to 12 morphisms influence the prognosis of leukemia after chemo- days, and DNR 40 mg/m2 was given on days 1 to 4, and if therapy. Recently it was reported that the null genotype of necessary, on days 10 to 12 in addition to the above schedule glutathione-S transferase theta 1 (GSTT1) was associated with for AML-87. In the AML-92 study,11 patients were randomized 7 prognosis in childhood acute myeloid leukemia (AML). to receive BHAC-DM similar to the AML-87 protocol with or In this study, we analyzed the prognostic significance of without etoposide (ETP, 100 mg/m2 for 5 days). After complete gene polymorphism of GSTT1, glutathione-S transferase mu remission (CR) was achieved, three courses of consolidation 1 (GSTM1), NAD(P)H:quinone oxidoreductase (NQO1) and chemotherapy and six courses of intensification chemo- therapy were given. Patients 60 years or older received about two-thirds of the dosage of each drug throughout the study Correspondence: T Naoe, Department of Infectious Diseases, Nagoya University School of Medicine, Tsurumai-cho 65, Showa-ku, Nagoya period. 466-8560, Japan; Fax: +81-52-744-2801 CR was defined as less than 5% blasts in normo-cellular Received 27 June 2001; accepted 12 October 2001 bone marrow with normal levels of peripheral neutrophils and GSTT1 genotype and early death in AML T Naoe et al 204 platelet counts. Overall survival was calculated from the first were 5-ACACAACTGTGTTCACTAGC-3 and 5-CAACTTCATC day of therapy to death. Disease-free survival (DFS) for CACGTTCACC-3. The MPO gene polymorphism located 463 patients who had achieved CR was measured from the date bp upstream of exon 1 in the promoter region was exam- of CR to relapse or death. Relapse-free survival was defined ined.12 Briefly, a 567-bp DNA fragment was amplified using as the time from the date of CR to relapse or death from pro- 5Ј-AGGCCAATTGGGTCATCTTTACTC-3Ј and 5Ј-GACGGTT gressive disease, censoring deaths from other causes. Patients ATCTTGCTCTGTT-3Ј, with a second amplification using 5Ј- who underwent bone marrow transplantation (BMT) were AGGAACCCTGGATAAACAGTGTAACC-3Ј and 5Ј-GCCTCTA censored from the date of BMT. GCCACATCATCAATT-3Ј. The reaction comprised 30 cycles of 94°C for 30 s, 55°C for 2 min and 72°C for 2 min. An additional cycle was performed at 72°C for 10 min. The final Genotyping PCR products were digested with AciI (New England Biolabs). In cases of G/G and A/A at 463, two fragments (189 and 154 The genotyping procedure for NQO1, GSTM1 and GSTT1 bp) and one fragment (343 bp) were obtained, respectively. was described previously.8 Briefly, for the amplification of the NQO1 gene fragment, the sense and anti-sense primers were 5-AGTGGCATTCTGCATTTCTGTG-3 and 5-GATGGACTT GCCCAAGTGATG-3, respectively. The amplification was car- Statistical analysis ried out in a thermocycler (model 9600; Applied Biosystems, Foster City, CA, USA) with an initial denaturation step (8 min, 95°C), followed by 35 cycles consisting of three steps: 94°C Survival probabilities were estimated by the Kaplan–Meier for 30 s, 56°C for 1 min and 72°C for 2 min. An additional method, and differences in the distributions between the cycle was performed at 72°C for 10 min. The amplified frag- genotypes were evaluated using the log-rank test. The prog- ments were digested with HinfI endonuclease (New England nostic significance of the clinical variables was assessed using Biolabs, Beverly, MA, USA) and analyzed on agarose gel the Cox proportional hazards model. These statistic analyses electrophoresis. The paired primers for GSTM1 and GSTT1 were performed with StatView software (Abacus Concepts, were 5-GAACTCCCTGAAAAGCTAAAGC-3 and 5-GTTGGG Berkeley, CA, USA). For all analyses, P values were two-tailed, CTCAAATATACGGTGG-3, and 5-TTCCTTACTGGTCCTCAC and a P value of less than 0.05 was considered significant. ATCTC-3 and 5-TCACCGGATCATGGCCAGCA-3, respect- Since CR rates, overall survival and DFS according to ively. The presence or absence of GST genes was determined induction therapy (AML-87, -89 and -92) did not show any by a differential PCR in which the ␤-globin gene was co- differences, the data of the three studies were combined and amplified in the same reaction tube. The primers for ␤-globin analyzed. Table 1 Clinical and molecular characteristics of 193 patients with de novo AML except M3 according to GSTT1 genotype Factora GSTT1+ GSTT1− P n = 124 n = 69 Clinical characteristic Age (y) median 50.5 47 0.56 Sex F 51 30 0.75 M7339 FAB M0 0 3 0.13 M1 33 13 M2 51 30 M4 28 17 M5 10 3 M6 2 2 M7 0 1 WBC median 24.4 24.3 0.8 (× 106/l) Karyotype favorable 20 13 0.59 intermediate 77 39 unfavorable 10 6 ND 17 11 Germ line polymorphism GST-M1 present 48 29 0.65 absent 76 40 NQO1 P/P 58 31 0.47 P/S 49 24 S/S 17 14 MPOb A/A 1 0 0.49 A/G 18 11 G/G 105 57 Therapy AML-87 16 10 0.54 AML-89 28 11 AML-92 80 48 aFactors.
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