[CANCER RESEARCH 62, 4100 – 4108, July 15, 2002]
Transcript Map of the 3.7-Mb D19S112–D19S246 Candidate Tumor Suppressor
Region on the Long Arm of Chromosome 19
1
Christian Hartmann, Loki Johnk, Gaspar Kitange, Yanhong Wu, Linda K. Ashworth, Robert B. Jenkins, and
David N. Louis
2
Molecular Neuro-Oncology Laboratory, Department of Pathology and Neurosurgical Service, Massachusetts General Hospital and Harvard Medical School, Boston,
Massachusetts 02129 [C. H., L. J., D. N. L.]; Division of Laboratory Genetics, Mayo Clinic and Foundation, Rochester, Minnesota [G. K., Y. W., R. B. J.]; and Lawrence
Livermore National Laboratory, Livermore, California and Department of Energy Joint Genome Institute, Walnut Creek, California [L. K. A.]
ABSTRACT
Allelic losses of the q13.3 region of chromosome 19 have been docu-
mented in malignant gliomas, neuroblastomas, and ovarian carcinomas,
strongly suggesting the presence of a 19q13.3 tumor suppressor gene.
Deletion mapping in tumors over the past decade has narrowed the
candidate region considerably but has produced partially conflicting re-
sults, with some small candidate regions defined only by isolated tumors
with deletions. Mutation and expression screening of genes from the most
likely candidate regions has failed to identify the gene of interest, perhaps
because of the conflicting deletion mapping data. The recently increased
public availability of human genomic sequence, combined with improved
bioinformatics capabilities, has now made it possible to map much larger
candidate regions in considerable detail. We have manually generated a
transcript map that spans most of the 19q13.3 tumor suppressor candidate
region, from D19S219 to D19S246, with a resolution and quality superior
to that of computer-generated maps. These results are presented in the
hope that an improved map of the candidate region will facilitate further
widespread screening and eventual identification of the gene or genes
deleted in human gliomas, neuroblastomas, and ovarian cancers.
INTRODUCTION
Allelic losses of the long arm of chromosome 19 in a variety of
human malignancies strongly suggest that 19q harbors a tumor sup-
pressor gene. Loss of 19q is found commonly in all three major types
of diffuse human malignant gliomas (1–5) as well as in epithelial
ovarian cancers and neuroblastomas (6 – 8). Indeed, this region is
already of clinical importance, because 19q loss in combination with
1p loss is associated with a greater likelihood of chemosensitivity,
more durable chemotherapeutic responses, and longer overall survival
in patients with anaplastic oligodendrogliomas (9 –11). There has,
therefore, been considerable interest in identifying the putative tumor
suppressor gene from this candidate region.
Deletion mapping studies of malignant gliomas have gradually
narrowed the candidate region over the past decade (Fig. 1). A
common region of loss in astrocytomas was initially found between
19q13.11 and 19q13.4 (12, 13) and was then reduced to a 9.5-Mb area
between D19S178 on 19q.13.2 and D19S180 on 19q13.4 (14) and to
a 4-Mb region on 19q13.3 between APOC1 and HRC (15). Subse-
quently identified 1.4-Mb deletion areas between D19S412 and STD
(16) and between D19S241E and D19S596 (17) defined a minimal
common deletion region of 150 kb (17). Sequencing of this 150-kb
candidate region revealed GLTSCR1, EDH2, GLTSCR2, and SW, but
no mutations or expression abnormalities were found in these genes
(18, 19). Recent deletion mapping in neuroblastomas has demon-
strated a commonly deleted region between D19S412 and D19S606,
overlapping the larger glioma candidate regions but excluding the
150-kb glioma candidate region (7). On the other hand, one glioma
has been reported with an interstitial loss of a 425-kb region between
D19S219 and D19S112 at 19q13.3 (20), centromeric to the probable
glioma/neuroblastoma locus. Conversely, epithelial ovarian cancer
deletions apparently overlap more telomerically on 19q13.3, between
D19S246 and the KLK gene family (8). There is thus controversy in
assigning the most likely location for the 19q tumor suppressor, with
some candidate regions based only on a small number of deletions in
genetically unstable tumors, and it remains possible that the region
contains more than one tumor suppressor locus. These difficulties
have thwarted identification of the gene, or genes, of interest.
Although traditional gene-hunting strategies required mapping a
region of interest to a few hundred kilobases, the public availability of
extensive draft sequences from the human genome and of computer
bioinformatics programs has made it possible to map much larger
candidate regions. This event has in turn raised the possibility that a
larger transcript map could be probed more effectively for the 19q
gene than smaller maps following more traditional approaches. Here
we present a manually generated transcript map that spans most of the
19q13.3 tumor suppressor candidate regions, from D19S219 to
D19S246, with a resolution superior to that of currently available
computer-based maps. The map covers a candidate region defined by
many tumor breakpoints, reducing the likelihood that genomic insta-
bility in individual tumors could direct gene identification strategies to
an incorrect locus. This large transcript map thus lays the groundwork
for the prioritization of 19q tumor suppressor gene candidates and the
determination of their involvement in these important human malig-
nancies by further high-throughput screening studies.
MATERIALS AND METHODS
Physical Map. An approximately 3.7-Mb physical map spanning
the region from D19S112 to D19S246 was generated using 28 BACs
3
and
19 cosmids/fosmids sequenced by LLNL (Table 1). Publicly available scaf-
folds GA_x2KMHMR58TM, GA_x2KMHMR58UK, GA_x2KMHMR58JG,
GA_x2KMHMR58W5, GA_x2KMHMR58UK, GA_x2KMHMR592L,
GA_x2KMHMR58HM, GA_x8WDQ41, GA_x8WDQ6N, GA_x8WDQ6T,
and GA_x8WDQ7U from Celera (Celera Genomics, Rockville, MD) were
then applied to control for sequence ordering and quality and also to fill gaps.
Results from an earlier shotgun sequencing project of the minimal deletion
region based on BAC 284K17 were also included (18). BAC and cosmid/
fosmid order was also accomplished using the chromosome 19q arm metric
physical map from LLNL.
4
Discrepancies were resolved within the human
genome BAC clone map, based on shared restriction fragments from the
Genome Sequence Center of Washington University School of Medicine, St.
Louis.
5
Sequence assembly was accomplished with SeqMan II 5.0 (DNAstar,
Madison, WI) and Staden-Package 2000.0.
6
Identification of Genes, CpG Islands, and Promoter Regions. Genes
were identified by two different strategies. Nucleotide similarity searches with
Received 3/1/02; accepted 5/9/02.
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.
1
Supported by NIH Grants CA69285 (to D. N. L.) and CA85799 (to R. B. J.).
2
To whom requests for reprints should be addressed, at Molecular Neuro-Oncology
Laboratory, CNY6, Massachusetts General Hospital, 149 Thirteenth Street, Charlestown, MA
02129. Phone: (617) 726-5510; Fax: (617) 726-5079; E-mail: louis@helix.mgh.harvard.edu.
3
The abbreviations used are: BAC, bacteria artificial chromosome; LLNL, Lawrence
Livermore National Laboratory; hEST, human expressed sequence tag.
4
Internet address: http://greengenes.llnl.gov/genome-bin/loadmap?region = mq.
5
Internet address: http://genome.wustl.edu/gsc/human/Mapping/index.shtml.
6
Internet address: http://www.mrc-lmb.cam.ac.uk/pubseq/staden_home.html.
4100
Research.
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