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Hamon Center for Therapeutic Oncology Research, University of Texas Southwestern Medical Center, Dallas, Texas 75390-8593 [J. D. M.], and Laboratory of Immunobiology, National Cancer Institute, Frederick Cancer Research and Development Center, Frederick, Maryland 21702 [M. I. L.]
We used overlapping and nested homozygous deletions, contig building,
genomic sequencing, and physical and transcript mapping to further
define a 
630-kb lung cancer homozygous deletion region harboring one
or more tumor suppressor genes (TSGs) on chromosome 3p21.3. This
location was identified through somatic genetic mapping in tumors,
cancer cell lines, and premalignant lesions of the lung and breast,
including the discovery of several homozygous deletions. The
combination of molecular manual methods and computational predictions
permitted us to detect, isolate, characterize, and annotate a set of 25
genes that likely constitute the complete set of protein-coding genes
residing in this 630-kb sequence. A subset of 19 of these genes was
found within the deleted overlap region of 370-kb. This region was
further subdivided by a nesting 200-kb breast cancer homozygous
deletion into two gene sets: 8 genes lying in the proximal 120-kb
segment and 11 genes lying in the distal 250-kb segment. These 19
genes were analyzed extensively by computational methods and were
tested by manual methods for loss of expression and mutations in lung
cancers to identify candidate TSGs from within this group. Four genes
showed loss-of-expression or reduced mRNA levels in non-small cell lung
cancer
(CACNA2D2/
2
-2,
SEMA3B [formerly SEMA(V),
BLU, and HYAL1] or small cell lung
cancer (SEMA3B, BLU, and
HYAL1) cell lines. We found six of the genes to have two
or more amino acid sequence-altering mutations including
BLU, NPRL2/Gene21, FUS1,
HYAL1, FUS2, and SEMA3B.
However, none of the 19 genes tested for mutation showed a frequent
(>10%) mutation rate in lung cancer samples. This led us to exclude
several of the genes in the region as classical tumor suppressors for
sporadic lung cancer. On the other hand, the putative lung cancer TSG
in this location may either be inactivated by tumor-acquired promoter
hypermethylation or belong to the novel class of haploinsufficient
genes that predispose to cancer in a hemizygous (+/-) state but do not
show a second mutation in the remaining wild-type allele in the tumor.
We discuss the data in the context of novel and classic cancer gene
models as applied to lung carcinogenesis. Further functional testing of
the critical genes by gene transfer and gene disruption strategies
should permit the identification of the putative lung cancer TSG(s),
LUCA. Analysis of the 630-kb sequence also provides
an opportunity to probe and understand the genomic structure,
evolution, and functional organization of this relatively gene-rich
region.
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