Role of Inherited Defects of MYH in the
Development of Sporadic Colorectal Cancer
Takeshi Kambara,
1,2
Vicki L. J. Whitehall,
1
Kevin J. Spring,
1
Melissa A. Barker,
1
Sven Arnold,
1
Coral V. A. Wynter,
1
Nagahide Matsubara,
2
Noriaki Tanaka,
2
Joanne P. Young,
1
Barbara A. Leggett,
1*
and
Jeremy R. Jass
3*
1
Conjoint Gastroenterology Laboratory, Royal Brisbane and Women’s Hospital Research Foundation and Queensland Institute of
Medical Research, Brisbane, Australia
2
Department of Gastroenterological Surgery, Okayama University Graduate School of Medicine and Dentistry, Okayama, Japan
3
Department of Pathology, McGill University, Montreal, Quebec, Canada
Biallelic germ-line variants of the 8-hydroxyguanine repair gene MYH have been associated with multiple colorectal adenomas
that display somatic G:C3 T:A transversions in APC. However, the effect of single germ-line variants has not been widely
studied. To examine the relationship between monoallelic MYH variants and susceptibility to sporadic colorectal cancer
(CRC), 92 cases of sporadic CRC, 19 cases of familial CRC not meeting the Bethesda guidelines, 17 cases with multiple
adenomas, and 53 normal blood donors were screened for 8 potentially pathogenic germ-line MYH variants. Loss of
heterozygosity (LOH) at 1p adjacent to the MYH locus, microsatellite instability (MSI) status, and somatic mutations in KRAS2
and APC were analyzed in sporadic cancers. Neither homozygote nor compound heterozygote MYH variants were observed
in the germ-line of any subjects with sporadic CRC. There was no difference in the incidence of monoallelic variants between
this group (20 of 92, 22%) and cancer-free controls (14 of 53, 26%). However, the presence of monoallelic germ-line MYH
variants was negatively associated with an MSI-high (MSI-H) tumor phenotype, with an incidence of only 1 of 23 (4%) MSI-H
CRCs as contrasted with 19 of 69 (28%) non-MSI-H (P = 0.02). Further, 4 of 5 tumors with 1p LOH contained monoallelic
MYH variants compared with 15 of 53 without 1p LOH (P = 0.04) and the normal population (P = 0.03). The presence of
G:C3 T:A transversions in KRAS2 or APC was significantly more common in single MYH variant tumors (9 of 12) than in MYH
wild-type tumors (11 of 33; P = 0.02). These results suggest that single germ-line variants of MYH may influence genetic
pathways in CRC. © 2004 Wiley-Liss, Inc.
INTRODUCTION
Colorectal cancer (CRC) arises from the accumu-
lation of multiple mutations in the oncogenes and
tumor-suppressor genes (TSGs) that support nor-
mal growth and differentiation in the colon (Fearon
and Vogelstein, 1990). Defects in DNA repair lead
to an increased frequency of mutations, thereby
increasing the likelihood that cancer will develop
(Jiricny and Marra, 2003). A deficiency in DNA
mismatch repair is known to be the basis for he-
reditary nonpolyposis colorectal cancer (HNPCC;
Fishel et al., 1993; Leach et al., 1993; Bronner et
al., 1994), and its associated tumor phenotype,
high-level microsatellite instability (MSI-H), also
has been demonstrated in approximately 15% of
sporadic CRC cases (Aaltonen et al., 1993; Kinzler
and Vogelstein, 1996). A subset of the remaining
sporadic CRC cases has exhibited low-level MSI
(MSI-L) in association with transcriptional silenc-
ing of the DNA repair gene MGMT by promoter
hypermethylation (Whitehall et al., 2001). Methyl-
ation and silencing of MGMT have also been asso-
ciated with G3 A transitions in KRAS2 and TP53 in
CRC (Esteller et al., 2000, 2001). However, the
mechanism underlying genetic instability in most
sporadic non-MSI-H CRC is unknown. Recently,
the human homologue of the base excision repair
(BER) gene MutY (MYH) has been implicated in
the causation of an adenoma-prone phenotype (Al-
Tassan et al., 2002). MYH is a DNA glycosylase
responsible for the removal from DNA of adenines
mispaired with 8-hydroxyguanine (8-OG), one of
the most mutagenic DNA products of oxidative
DNA damage (Slupska et al., 1996; Hayashi et al.,
2002). In a study by Parker et al. (2002), 33% of
microsatellite stable (MSS) CRC cell lines ana-
Supported by: in part, Royal Brisbane and Women’s Hospital
Research Foundation; Australian National Health and Medical Re-
search Council; U.S. National Institutes of Health; Grant number:
UO1-CA74778; Walter Paulson Memorial Tumor Bank.
*Correspondence to: Barbara A. Leggett or Jeremy R. Jass.
E-mail: barbara_leggett@health.qld.gov.au
E-mail: jeremy.jass@mcgill.ca
Received 19 September 2003; Accepted 16 December 2003
DOI 10.1002/gcc.20011
Published online 26 February 2004 in
Wiley InterScience (www.interscience.wiley.com).
GENES, CHROMOSOMES & CANCER 40:1–9 (2004)
RESEARCH ARTICLE
© 2004 Wiley-Liss, Inc.