ICANCER RESEARCH 58. 2456-2460. June I, 1998]
Identification of Two Common Regions of Allelic Loss in Chromosome Arm 12q in
Human Pancreatic Cancer1
Mitsuhiro Kimura,2 Toni Furukawa,2 Tadayoshi Abe, Toshimasa Yatsuoka, Emile M. Youssef, Tadaaki Yokoyama,
Hong Ouyang, Yasuyuki Ohnishi, Makoto Sunamura, Masao Kobari, Seiki Matsuno, and Akira Horii3
Departments of Molecular Pathology ¡M.KL. T. F.. T. A., T. Ya.. E. M. Y.. T. Yo., H. O., A. H.¡ and Surgery I ¡M.KL, T. A., T. Ya.. T. Yo.. M. S.. M. Ko., S. M.], Tohoku
University School of Medicine, Sendai, 980-8575: Venture Business Laboratory, Tohoku University, Sendai, 980-8576 /£.M. Y.j: and Central Institute for Experimental Animals.
Kawasaki. 213-0027 ¡Y.O.¡,Japan
ABSTRACT
Using the method of microsatellite analysis, we studied 40 tissues with
pancreatic (liutai adenocarcinoma and identified two commonly deleted
regions on the long arm of chromosome 12. One (region A) was found
between D12S81 and D12S1719 at 12q21 at a frequency of 67.5%, and the
other (region B) was located between DÌ2S360and D12S78 at 12q22-
q23.1 at a frequency of 60%; the latter was reported previously (M.
Kimura, et al. Genes Chromosomes Cancer, 17: 88-93, 1996). The results
of microsatellite analyses were verified by fluorescence in situ hybridiza
tion. We further analyzed 19 pancreatic cancer cell lines by fluorescence
in situ hybridization and found that 10 of them showed allelic loss at
D12S81 and 6 showed allelic loss at D12S360. Yeast artificial chromosome
contigs were constructed to cover the deleted regions. Region B was
completely covered by a 650-kb yeast artificial chromosome clone. The
frequently deleted regions in chromosome 12q in pancreatic cancer that
were identified here may provide new avenues for isolating novel tumor
suppressor genes.
INTRODUCTION
Pancreatic cancer is one of the leading causes of cancer death in
Japan, as well as in Western countries. The poor prognosis is due to
difficulty in diagnosis and inefficiency in surgical and/or multidisci-
plinary treatment of the cancer ( 1). An understanding of the molecular
mechanisms of pancreatic carcinogenesis would provide important
molecular clues for the development of methods for early detection
and efficient therapy of this very malignant disease. Recent cytoge-
netic studies using karyotype analyses, as well as microsatellite anal
yses, CGH,4 and FISH, suggest that many genetic alterations occur in
several chromosomal regions other than those including MTS1, p53,
and DPC4 (2-11). These results suggest possible involvement of
unknown genes in pancreatic carcinogenesis. We previously per
formed an allelotype analysis to search for localization of putative
tumor suppressor genes and identified a 1-cM region of common
allelic loss in 12q22-q23.1 (12). However, our CGH analysis sug
gested the existence of a region of common allelic loss in 12q other
than the one that we had identified by microsatellite analysis (13).
Hence, we examined the entire region on the long arm of chromosome
12 with microsatellite analysis and FISH combined to construct a
deletion map of the entire chromosome 12q arm in pancreatic ductal
Received 11/26/97; accepted 4/2/98.
The costs of publication of this article were defrayed in part by the payment of page
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18 U.S.C. Section 1734 solely to indicate this fact.
1This work was supported in part by the Ministry of Education. Science, Sports and
Culture of Japan, the Vehicle Racing Commemorative Foundation, the Japanese Foun
dation for Multidisciplinary Treatment of Cancer, the Mitsui Life Social Welfare Foun
dation, the Terumo Life Science Foundation, the Sagawa Foundation for Promotion of
Cancer Research, and the Pancreas Research Foundation of Japan.
- The first two authors contributed equally to this work.
' To whom requests for reprints should be addressed, at Department of Molecular
Pathology, Tohoku University School of Medicine, Sendai. 980-8575, Japan. Phone:
81-22-717-8042; Fax: 81-22-717-8047; E-mail: horii@mail.cc.tohoku.ac.jp.
4 The abbreviations used are: CGH, comparative genomic hybridization; FISH, fluo
rescence i/i situ hybridization; LOH. loss of heterozygosity; BAC, bacterial artificial
chromosome; YAC, yeast artificial chromosome; STS, sequence-tagged site.
adenocarcinoma. Herein, we report identification of the two distinct
regions of common allelic loss in 12q in human pancreatic cancer.
MATERIALS AND METHODS
Tissues and Cell Lines. The materials studied were from 40 cases of
primary pancreatic ductal adenocarcinoma (23 men and 17 women, ages
31-81 years; mean age = 63.5 years). Thirty-three cases were surgically
resected, and 7 were obtained at autopsy. The average survival period after
diagnosis was 15.1 months. According to the clinical staging system of the
Japan Pancreas Society (14), 2 cases were in stage II, 9 were in stage III, and
28 were in stage IV. A brief explanation of the clinical staging system of the
Japan Pancreas Society was included in our previous report (13). In one case,
no description of the clinical stage was available. Histológica! diagnoses of the
tumors were as follows: 35 tubular adenocarcinomas, 2 papillary adenocarci-
nomas, 2 adenosquamous carcinomas, and 1 anaplastic carcinoma. Of the 40
tissues, 37 specimens were formalin-fixed, paraffin-embedded tissues, and 3
were frozen tissues. Tissues were cut to provide 13-15 20-/nm-thick sections
for microdissection. These sections were sandwiched between two 3-/j.m-thick
sections that were stained with H&E for histopathological examination. Under
a microscope, tumor cells were carefully dissected from the 20-/xm-thick
sections that had been deparaffmized, hydrated, and stained with hematoxylin.
In each sample, normal cells were also collected from the adjacent normal
tissue. DNAs were extracted from the dissected tissues, as described previ
ously (12). Nineteen pancreatic cancer cell lines, PK-1, PK-8, PK-9, PK-59.
PCI-6. PCI-10, PCI-19, PCI-35, PCI-43, PCI-64, PCI-66, PAN02JCK.
PAN03JCK, PAN07JCK, PAN09JCK, Panc-1, MIA PaCa-2, SU.86.86, and
BxPc-3, were cultured as described (15-24). The primary tumors from which
these cell lines derived were not available.
Microsatellite Analysis. Allelic imbalances were detected by the micro-
satellite analysis method in 40 tissues, as described previously (12). Twenty-
four microsatellite markers were used, as listed in Fig. 2, to cover the entire
long arm of chromosome 12. Detailed information on the primers and PCR
conditions used is available upon request. The primers were end-labeled with
[12P]ATP with polynucleotide kinase (New England Biolabs, Beverly. MA)
and used for PCR. The amplified products were fractionated in a gel composed
of 6% polyacrylamide, 8 M urea, and 32% formamide and then autoradio-
graphed. Relative intensities of allele-specific bands were examined by quan
titative densitometry using NIH Image software (details of this software
are available at: http://cbel.dcrt.nih.gov/~mvivino/ImgEngrHTML/ImgEngr.
html). LOH was defined as 50% or more reduction in relative intensity in one
allele-specific band, as compared to the band of the normal counterpart.
Homozygous alÃ-eles,microsatellite instabilities, and poor yield of PCR prod
ucts for each marker were not scored in this study.
Construction of Contigs Using BAC and YAC. DNA superpools of YAC
and BAC libraries (Research Genetics, Huntsville, AL) were screened by PCR
with primers for the microsatellite markers, according to the manufacturer's
instructions. BAC and YAC clones that were positive for microsatellite mark
ers were purchased from Research Genetics. Agarose plugs of YACs and
BACs were prepared and analyzed for their sizes using the CHEF Mapper
pulsed-field gel electrophoresis system (Bio-Rad. Hercules. CA), according to
the manufacturer's instructions. Total yeast DNA, including YAC, was puri
fied by the methods described (25). Cosmid libraries were generated from the
DNAs of YACs and screened to select clones that harbor human sequences by
colony hybridization with total human DNA as the probe (26). Cosmid clones
harboring microsatellite markers were detected by hybridization with end-
labeled oligonucleotide primers that were used for PCR amplifications. A
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Research.
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