ICANCERRESEARCH57.4164-4166. October1, 1997]
Advances in Brief
Genetic Mapping of Lung Cancer Modifier Loci Specifically Affecting Tumor
Initiation and Progression'
Giacomo Manenti, Manuela Gariboldi, Antonio Fiorino, Nicola Zanesi, Marco A. Pierotti, and Tommaso A. Dragani2
Division of Experimental Oncology A, istituto Nazionale per lo Studio e Ia Cura dei Tumori, 20133 Milan, italy
affect lung tumor multiplicity. In the same cross, we have also
mapped, on chromosome 4, a locus designated as Papgl specifically
affecting the size of lung tumors.
Materials and Methods
Animals and Phenotype. Male and female SWR/J (W) and BALB/cJ (C)
mice were purchased from The Jackson Laboratory (Bar Harbor, ME). Mice
were then bred in our laboratory to obtain CWF2 mice, which were given a
single i.p. injection of 1000 mg of urethane dissolved in water (BDH Chem
icals, Poole, United Kingdom) per kg body weight CWF2 male and female
mice were killed at 40 weeks of age. The number of tumors on the surface of
the lungs were counted after tissue fixation, and the diameter of each nodule
was measured. Susceptibility of each mouse to lung tumor development was
estimated using quantitative parameters, as described (7).
Genetic Markers and Linkage Analysis. Primers for simple sequence
length polymorphism markers were obtained from Research Genetics (Hunts
ville, AL). Forty mice showing extreme phenotypes were genotyped with 231
markers covering all autosomes and chromosome X. Markers located on
chromosomes showing putative linkage were typed in the whole CWF2 pop
ulation (218 mice). Genetic linkage maps and linkage between parameters
estimating lung cancer predisposition trait and genetic markers were deter
mined as reported (3, 8, 9). Because the susceptible phenotype showed a
nonnormal distribution, the linkage methods were applied to rank-transformed
data (10), although the phenotypic values reported in Table 1 refer to untrans
formed data.
Results
Loci Specifically Affecting Tumor Multiplicity. Whole-genome
scanning of 40 extreme-phenotype mice with 23 1 markers showed
significant linkage of a chromosome 18 region with lung tumor
multiplicity (N). The lod score curve peaked at the Dl8Mit9 locus at
42 cM (Ref. 11; Fig. 1). The linkage between the Dl8Mit9 region and
N was supported by a led score of 7.9. Mean lung tumor volume (V)
showed only a marginal linkage at the same locus (led score of 2.1).
ANOVA confirmed the linkage (P < 0.0001) between lung tumor
multiplicity and Dl8Mit9, which explained —15% of the total phe
notypic variance (Table 1). Values of lung tumor multiplicity by
genotypic class at Dl8Mit9 indicate that BALB/c mice carry the
resistance allele (Par2/+), and SWR/J mice carry the susceptibility
allele (Par2/—). Resistance to multiplicity oflung cancer by Par2 was
partially dominant, because heterozygous CWF2 animals showed an N
value lower than the expected intermediate value for genetic effect of
additive alleles but higher than that of the homozygous mice for the
BALB/c allele (Table 1). The use of an intercross as compared to a
backcross population had the advantage of allowing analysis of locus
inheritance mode (i.e., partially dominant). The weak effect of Par2
on lung tumor size (V) behaved as a recessive trait, because only mice
homozygous for the BALB/c allele showed a reduced V value, and
heterozygous animals were not affected (Table 1).
Therefore, Obata et a!. (6) and we have identified another locus
(Par2) providing inherited resistance to lung tumorigenesis. However,
in our CWF2 cross, Par2 accounts for about 15% of the phenotypic
variance, whereas in the (A/i X BALB/c) X NJ backcross used by
Abstract
Mouse inbred strains with inherited predisposition and resistance to
lung cancer provide a tool for the dissection of the complex genetics of this
disease. In the present report, we have crossed the BALB/C with the
SWR/J strain and performed whole-genome scanning for loci affecting
lung tumor development in their F2 progeny. Both parental strains carry
the pulmonary adenoma susceptibility 1 (Pasi) locus, a major locus af
fecting predisposition to lung cancer in mice. On distal chromosome 18
and on centromere of chromosome 6, we have mapped two pulmonary
adenoma resistance loci (Par2 and Par4, respectively), which reduce lung
tumor multiplicity strongly, up to 15-fold. Par2 and Par4, however, do not
affect lung tumor size, which is instead controlled by an additional locus
that we have mapped on the central region of chromosome 4. We desig.
nated this locus as â€oepulmonary adenoma progression 1― (Papgl), because
it specifically modifies lung tumor size but not multiplicity. The present
results, therefore, provide evidence for the existence of cancer modifier
loci acting on specific stages of lung tumorigenesis
Introduction
In the last few years, progress in the genetics of an inherited
predisposition to lung cancer in mice demonstrated that a major locus
(Pasi) located on the distal region of chromosome 6 affects suscep
tibility to lung tumorigenesis (1). Other minor loci may also contribute
to the susceptibility trait (2). Recently, we have reported the mapping
of a Mus spretus-derived locus that strongly inhibits the lung tumor
igenesis in Pasl/+ mice (3). This locus, pulmonary adenoma resist
ance 1 (Pan), maps on mouse chromosome 11, near the Rara locus
(3). These findings provided the first evidence for the existence of a
lung tumor resistance locus inhibiting the expression of an inherited
predisposition to lung cancer.
To further define the genetics of predisposition and resistance to
lung cancer in mice, we have considered the BALB/c strain, which
shows an intermediate susceptibility that is dominant over the high
susceptibility of the A/J and SWR strains (4). Given that all three
strains carry the Pasl/+ allele (5), the BALB/c mouse must carry lung
tumor modifier loci that decrease expression of high susceptibility to
lung tumorigenesis. Therefore, a cross between the BALB/c and one
of the most susceptible strains would provide a clue to map lung
cancer modifier loci in a common genetic background for Pasi.
Accordingly, in a cross between the BALB/c and the SWRJJ mice,
here we report the mapping of BALB/c-derived pulmonary adenoma
resistance (Par2 and Par4) loci, on chromosomes 18 and 6. Our
findings are in agreement with a recent report mapping the same Par2
locus on the distal region of chromosome 18 (6). Both loci specifically
Received 7/14/97; accepted 8/8/97.
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
18U.S.C.Section1734solelyto indicatethisfact.
I This work was supported in part by grants from Associazione and Fondazione
Italiana Ricerca Cancro.
2 To whom requests for reprints should be addressed, at Istituto Nazionale Tumori, Via
G. Venezian 1, 20133 Milan, Italy. Fax: 39-2-2390764; Phone: 39-2-2390642;, E-mail:
dragani@istitutotumori.mi.it.
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