5,10-Methylenetetrahydrofolate Reductase Polymorphisms
and Acute Lymphoblastic Leukemia Risk: A Meta-analysis
Tiago Veiga Pereira,
1
Martina Rudnicki,
2
Alexandre Costa Pereira,
3
Maria S. Pombo-de-Oliveira,
4
and Rendrik Franc ¸aFranco
5
1
Department of Biochemistry and Molecular Biology, Federal University of Sa ˜o Paulo;
2
Clinical and Toxicological Analysis Department,
Faculty of Pharmaceutical Sciences, and
3
Heart Institute (Instituto do Corac ¸a ˜o),Sa ˜o Paulo University Medical School,
University of Sa ˜o Paulo;
4
Division of Experimental Medicine, Instituto Nacional de Ca ˆncer, Rio de Janeiro,
Rio de Janeiro, Brazil; and
5
Fleury Research Institute, Sa ˜o Paulo, Sa ˜o Paulo, Brazil
Abstract
There is evidence supporting a role for 5-10 methylenetetra-
hydrofolate reductase (MTHFR ) gene variants in acute
lymphoblastic leukemia (ALL). To provide a more robust
estimateoftheeffectof MTHFR polymorphismsontheriskof
ALL, we did a meta-analysis to reevaluate the association
between the two most commonly studied MTHFR polymor-
phisms (C677T and A1298C) and ALL risk. All case-control
studies investigating an association between the C677T or
A1298C polymorphisms and risk of ALL were included. We
applied both fixed-effects and random-effects models to
combine odds ratio (OR) and 95% confidence intervals
(95% CI). Q-statistic was used to evaluate the homogeneity
andbothEggerandBegg-Mazumdartestswereusedtoassess
publication bias. The meta-analysis of the C677T polymor-
phismandriskofchildhoodALLincluded13studieswitha
totalof4,894individuals.Underafixed-effectsmodel,theTT
genotypefailedtobeassociatedwithastatisticallysignificant
reductionofchildhoodALLrisk(TTversusCT+CC:OR,0.88;
95% CI, 0.73-1.06; P = 0.18). However, individuals homo-
zygousforthe677Talleleexhibiteda2.2-folddecreaseinrisk
ofadultALL(TTversusCT+CC:OR,0.45;95%CI,0.26-0.77;
P = 0.004). In both cases, no evidence of heterogeneity
was observed. No association between the A1298C variant
and susceptibility to both adult and childhood ALL was
disclosed.Ourfindingssupporttheproposalthatthecommon
geneticC677Tpolymorphisminthe MTHFR contributestothe
risk of adult ALL, but not to the childhood ALL susceptibi-
lity. (CancerEpidemiolBiomarkersPrev2006;15(10):1956–63)
Introduction
Acute lymphoblastic leukemia (ALL) is the commonest
pediatric cancer in industrialized countries (1, 2). With an
incidenceexpectedtoreachupto4.75casesper100.000people
worldwide, ALL represents f80% of leukemia diagnoses (2).
Whereas ALL accounts for 23% of cancers among children
younger than 15 years, it is responsible for up to 20% of all
adultleukemias,whicharecharacterizedbyaworseprognosis
with a decreased long-term survival (2, 3). Although a
significant improvement in both ALL diagnosis and treatment
has been made over the past decades, the etiology of most
cases of ALL remains unknown due to probable multifactorial
mechanisms of pathogenesis (4). Recently, however, molecular
epidemiologic case-control studies suggest that both adults
and children harboring variant alleles of the 5,10-methylenete-
trahydrofolate reductase (MTHFR ) gene might have a de-
creased risk of ALL development (5).
The gene coding for MTHFR enzyme is located at
chromosome 1.p36.3 and composed of 2.2 kilobases with a
total of 11 exons (6). Despite the fact that several MTHFR
polymorphisms have been described thus far, only two
polymorphisms, C677T and A1298C, have been intensively
investigated. The C-to-T transition at the nucleotide position
677 in exon 4 of MTHFR generates an alanine-to-valine
substitution at amino acid 222. This substitution lies at the
binding site for the flavin adenine dinucleotide (7), an
important cofactor for MTHFR. As a result, carriers of the
MTHFR 677TT genotype possess a thermolabile enzyme of
reduced activity (8), with a subsequent mild decrease in both
serum and plasma folate and an increase in homocysteine
levels (5, 9). The second most studied polymorphism in
MTHFR is an A-to-C transversion substitution at nucleotide
1,298 (exon 7) that results in an amino acid substitution of
glutamate for alanine at codon 429 (10). Once this amino acid
substitution takes place at the S -adenosylmethionine regula-
tory domain of the MTHFR, the A1298C polymorphism also
generates an enzyme with a decreased activity (10). However,
in contrast to the C677T variant, biochemical observations
indicate that individuals homozygous for the 1298C allele do
not seem to have higher serum homocysteine levels or any
modification in folate status when compared with the wild-
type genotype (9).
The biological mechanism by which MTHFR variants are
thought to be associated with the ALL risk modulation is
related to a more efficient DNA synthesis (5). Because folate
playsamajorroleinnormalhumancellgrowthandleukemias
commonly arise as a result of DNA translocations, inversions,
or deletions in regulatory genes of the blood cell development
and homeostasis (4, 5, 11), a decreased MTHFR activity might
resultinanalterationofthenormalintracellulardistributionof
folate substrates (12). As a result, the folate precursors
pathway would be directed for purine and pyrimidine
synthesis, generating a reduced uracil misincorporation (13)
with a subsequent decreased number of genetic mutations and
a more stable DNA synthesis. Despite the appealing biological
mechanism, results on the relation between MTHFR poly-
morphisms and ALL risk are derived mainly from underpow-
ered studies and yielded conflicting results. To investigate the
possible effect of MTHFR variants on the ALL risk through a
more robust and powered analysis, we did a meta-analysis of
13 molecular epidemiologic case-control studies that examined
1956
Cancer Epidemiol Biomarkers Prev 2006;15(10). October 2006
Received 4/24/06; revised 7/7/06; accepted 7/19/06.
Grant support: Coordenac ¸a ˜o de Aperfeic ¸oamento Pessoal de Nı ´vel Superior and scholarship
CNPq #308532/2003-1 (M.S. Pombo-de-Oliveira).
The costs of publication of this article were defrayed in part by the payment of page charges.
This article must therefore be hereby marked advertisement in accordance with 18 U.S.C.
Section 1734 solely to indicate this fact.
Requests for reprints: Tiago V. Pereira, Department of Biochemistry and Molecular Biology,
Federal University of Sa ˜o Paulo, Instituto do Corac ¸a ˜o, Avenida Dr. Ene ´as de Carvalho
Aguiar 44, CEP 05403-000, Sa ˜o Paulo, SP, Brazil. Phone: 55-11-3069-5068; Fax: 55-11-3069-5068.
E-mail: t27026t@yahoo.com.br
Copyright D 2006 American Association for Cancer Research.
doi:10.1158/1055-9965.EPI-06-0334
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