[CANCER RESEARCH 58. 2107-2110. May 15. IWX]
Genetic Polymorphisms in Catechol-0-Methyltransferase, Menopausal Status, and
Breast Cancer Risk1
Patricia A. Thompson, Peter G. Shields, Jo I.. Freudenheim, Angie Stone, John E. Vena, James R. Marshall,
Saxon Graham, Rosemary Laughlin, Takuma Nemoto, Fred F. Kadlubar, and Christine B. Ambrosone2
Division of Molecular fyiidetniolof>y. National Center for Toxicological Research. Jefferson, Arkansas 72205 {P.A. T., A. S., F. F. K., C.B.AJ; Ltiboratory irf Human
Carcinogenesis, National Cancer Institute. Betliesda. Maryland 20X92 ¡P.G. S. /; Department of Social & Preventive Medicine. State University of New York at Buffalo. Muffalo,
New York 14214 ¡J.L F.. J. E. V., S. G., K. L. T. N.J: and Ari-unti Cancer Center. Tucson. Ari-ona 85724 ¡J.R. MJ
ABSTRACT
Polymorphic catechol-0-methyltransferase (COMT) catalyzes the O-
methylation of estrogen catechols. In a case-control study, we evaluated
the association of the low-activity alÃ-ele(COM7"M") with breast cancer
risk. Compared to women with CO/V/7"VlilAal, COMj*t"/M" was associated
with an increased risk among premenopausal women [odds ratio (OR),
2.1; confidence interval (CI), 1.4-4.3] but was inversely associated with
postmenopausal risk (OR, 0.4; CI, 0.2-0.7). The association of risk with at
least one low-activity COMT*1" alÃ-elewas strongest among the heaviest
premenopausal women (OR, 5.7; CI, 1.1-30.1) and among the leanest
postmenopausal women (OR, 0.3; CI, 0.1-0.7), suggesting that COMT,
mediated by body mass index, may be playing differential roles in human
breast carcinogenesis, dependent upon menopausa! status.
INTRODUCTION
It is widely believed that estrogen exposure is an important etio-
logical agent in breast carcinogenesis. However, studies of excreted
estrogens or estrogen metabolites have demonstrated only weak as
sociations between high levels of plasma or urinary estrogens and
breast cancer risk (1-3). The catechol estrogens (i.e., 2-hydroxy
estrogens) are the major metabolites of estrogens in humans and
animals (4). The 2- and 4-catechol estrogens have been reported to
demonstrate both cancer-promoting and -inhibiting activities through
interactions with the estrogen receptor or with macromolecules (i.e.,
cellular proteins and DNA; Refs. 3-9). Interindividual differences in
steroid metabolism have been noted and attributed to both genetic
polymorphisms in and differential expression of metabolizing en
zymes that hydroxylate and conjugate the steroid hormones (4, 10-
12). COMT3 is one of several phase II enzymes involved in the
conjugation and inactivation of the catechol estrogens (13). COMT is
found in various mammalian tissues, with high levels in liver and
kidney and significant amounts in RBCs. endometrium, and breast
( 14). An amino acid change (valine to methionine) at position 158/108
in the membrane-bound/cytosolic form of the protein has been linked
to decreased methylation activity of the enzyme (15). This amino acid
change is believed to be closely associated with the observed trimodal
distribution of COMT enzyme activity in the human population as
sociated with high COMrVill/Val. intermediate COMTVMMa. and low
COMT COMTMct/M" activity toward certain combination therapeu-
Received 11/24/97; accepted 3/19/98.
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' This work was a collaborative effort by the Division of Molecular 1-pidemiology.
National Center for Toxicological Research, the Department of Social and Preventive
Medicine, State University of New York at Buffalo, and Ihe Laboratory of Human
Carcinogenesis. National Cancer Institute. This work was supported, in part, by Grants
CAI 1535. CA/ES62995. and CA01633 from the National Cancer Institute and the
National Institute for Environmental Health Sciences and USAMRMC#CAMC17-°4-J-
4108. This work is solely Ihe responsibility of the authors and does not necessarily
represent the views of the National Cancer Institute.
2 To whom requests for reprints should be addressed, at Division of Molecular
Epidemiology. National Center for Toxicological Research. 39(X) NCTR Road. Jefferson.
AR 7207". K-mail:camhrosone<!*nctr.fda.gov.
'The abbreviations used are: COMT. catechol (J-methyltransferasc; BMI. body mass
index; OR, odds ratio; CI. confidence interval; HRT. hormone replacement therapy.
tics used in Parkinson's disease (16. 17). Because the genetic poly
morphism in COMT correlates with decreased enzyme activity and
because COMT is a major conjugation pathway for the catechol
estrogens, we sought to determine whether polymorphisms in Ihe
COMT gene may be associated with increased risk of breast cancer
and whether the association between genotypes and risk may be
modified by menopausa! status and body mass index.
MATERIALS AND METHODS
Study Population. These research dala were collected from an earlier
case-control study (1986-1991) of 617 premenopausal and 933 postmeno
pausal Caucasian women in Western New York; the detailed methods have
been reported (18. 19). The protocol for the study was reviewed by the
Institutional Review Board of the State University of New York at Buffalo and
of all of the participating hospitals. Informed consent was received from all
participants for interview and medical record review. Women diagnosed with
incident, primary, histologically confirmed breast cancer were frequency-
matched by age and county of residence with controls randomly selected from
the New York State Motor Vehicle lists (<65 years) and the Health Care
Finance Administration rolls (>65 years). Interview data included medical,
reproductive, and lifestyle histories. Approximately 45% of premenopausal
and 63% of postmenopausal women provided blood samples. DNA was
extracted from blood clots, as reported previously, and analy/ed tor COMT
genotype in case and control specimens having adequate DNA.
Laboratory Analysis. To determine the polymorphic COMT genotype.
DNA was subjected to PCR as described (20). Briefly. Ihe reaction conditions
included buffer [ 10 mM Tris-HCI (pH 8.3). 50 mM KC1], 2 IHMMgC12. 0.2 mM
2'-deoxynucleoside-3'-lriphosphate (Boehringer Mannheim. Indianapolis In
diana)]. 2.5 units ol Taq DNA polymerase (Promega Corp.. Madison. Wl). and
primers specific for COMT (10 pmol each; 5'-ACTGTGGCTACTCAGCT-
GTG-3' and 5'-CCTTTTTCCAGGTCTGACAA-.V) in a total reaction volume
of 100 fi\ using 100 ng of sample DNA. PCR producÃ-s( 169 bp) were digested
with Hsp92II (Promega) and analyzed by gel electrophoresis (2.5% Metaphor
agarosc; FMC BioProducts. Rockland. ME). Digestion of the COMT product
with Hsp92II gives rise to fragment sizes of 114. 23. and 32 bp for the
high-activity alÃ-eleand 96. 23. 32. and 18 bp for Ihe low-activity alÃ-ele.This
assay was validated hy confirming inheritance patterns in eight family lines
encompassing three generations (National Institute General Medical Scientist
Human Genetic Mutant Cell Repository; Coriell Institute. Camdcn. NJ). All
assays were conducted and interpreted by two reviewers (P. T. and A. S.)
blinded to case-control status.
Statistical Analysis. Student's i tests were performed to assess mean
differences in reproductive and lifestyle factors by COMT genotypes within
case and control groups. ORs and 95% CIs were calculated using unconditional
logistic regression to evaluate associations between COMT genotypes and
breast cancer risk separately for premenopausal and postmenopausal women.
ORs were adjusted for age. education, age at menarche. age at first pregnancy,
reported family history of breast cancer, body mass index, and age at meno
pause for postmenopausal women. Possible modification of risk by body muss
was evaluated by calculating ORs for genotype and breast cancer risk within
fertiles of body mass index, determined by the distribution among controls.
RESULTS
Genotype data for COMT were available for 281 women with
breast cancer and 289 community controls. For the most part, asso-
2107
Research.
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