[CANCER RESEARCH 47, 6294-6296, December 1. 1987)
Inheritance of Susceptibility to Phototumorigenesis and Persistent Hyperplasia in
F, Hybrids between SENCAR Mice and BALB/c or C57BL/6 Mice1
Paul T. Strickland2 and Rodney P. Swartz
Department of Environmental Health Sciences, The Johns Hopkins University, School of Hygiene and Public Health, Baltimore, Maryland 21205 fP. T. S.J, and
Pulmonary Disease Division, Georgetown University Hospital, Washington, DC 20007 [R. P. S.J
ABSTRACT
SENCAR mice are selectively bred for hypersusceptibility to two-
stage chemical skin carcinogenesis. They are also hypersusceptible to
UV radiation tumorigenesis with single high-dose, but not chronic low-
dose, exposures. In addition, SENCAR mice exhibit an exaggerated and
persistent epidermal hyperplasia (due to sustained proliferation of the
basal cells) in response to UV-induced tissue damage. In the present
study, we have examined the inheritance of susceptibility to both photo-
tumorigenesis and persistent hyperplasia in the l;, offspring of SENCAR
mice crossed with either of two inbred strains (BALB/c or C57BL/6)
which are relatively resistant to phototumorigenesis. A total of 428 mice
from the parental strains and reciprocal I-, crosses were given a single
high dose (8.64 x IO4 .l/iir) of UV radiation (FS40 sunlamps) which
causes persistent hyperplasia and tumorigenesis in many SENCAR, but
no BALB/c or C57BL/6, mice. F, hybrids between SENCAR and
C57BL/6 mice did not develop persistent hyperplasia or skin tumors,
which indicates that susceptibility to both traits is completely recessive
to the C57BL/6 genotype. In contrast, F, hybrids between SENCAR and
BALB/c mice developed both persistent hyperplasia and skin tumors,
although at a much lower incidence than the SENCAR mice, indicating
that susceptibility to both traits is only partially (incompletely) recessive
to the BALB/c genotype. Thus, in either I , cross, susceptibility to
phototumorigenesis decreased in parallel with persistent hyperplasia.
These results are consistent with the hypothesis that the two character
istics are mechanistically related.
INTRODUCTION
Exposure to exogenous carcinogens is believed to cause the
majority of human cancers. However, the considerable variation
within the human population for susceptibility to genotoxic
agents and carcinogenesis suggests that certain host factors
mediate this response (1, 2). Abnormalities in DNA repair or
oxidative metabolism have been associated with increased sus
ceptibility to carcinogenesis in some cases (3-5). One approach
directed toward understanding the mechanisms responsible for
susceptibility has been the study of animal strains unusually
susceptible to carcinogenesis. SENCAR mice are selectively
bred for hypersusceptibility to two-stage chemical skin carci
nogenesis (6-8) and are also hypersusceptible to UV radiation
carcinogenesis (9) with certain exposure protocols. While the
biological basis for this sensitivity is unclear, it probably does
not involve abnormalities in carcinogen metabolism (7, 8),
DNA repair (10, 11), epidermal growth factor receptors (12),
phorbol ester receptors ( 13), or systemic immunological factors
(14).
On the other hand, two anomalous properties of SENCAR
skin have been reported, (a) Cultured keratinocytes from SEN-
Received 5/13/87; revised 8/17/87; accepted 8/31/87.
The costs of publication of this article were defrayed in part by the payment
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1Research supported in part by funds from the Mellon Foundation and
Department of Health and Human Services Grants ES03841 and ES03819 and
in part by the National Cancer Institute. Department of Health and Human
Services, under Contract N01-CO-23909 with Litton Bionetics, Inc.
2To whom requests for reprints should be addressed, at Division of Occupa
tional Medicine, The Johns Hopkins University, 3100 Wyman Park Drive,
Building 6, Baltimore, MD 21211.
CAR skin are resistant to forced terminal differentiation by
modulation of Ca2+ concentration in the medium (15), whereas
keratinocytes from other (resistant) mouse strains are suscep
tible to forced differentiation, (b) SENCAR mice exhibit an
exaggerated and persistent epidermal hyperplasia (which is due
to sustained proliferation of epithelial basal cells) in response
to tissue damage caused by UV radiation (16). It is not known
whether these two properties are causally related to each other,
or to the hypersusceptibility of SENCAR mice to skin carci
nogenesis.
In the present study, the inheritance of susceptibility to
phototumorigenesis and persistent hyperplasia has been exam
ined in the F, offspring of SENCAR mice crossed with either
of two inbred strains (BALB/c or C57BL/6) which are relatively
resistant to phototumorigenesis. In addition, the distribution of
skin tumors and persistent hyperplasma among individual
SENCAR mice exposed to UV radiation was analyzed.
MATERIALS AND METHODS
Animals. Parental strains of mice [CnORL SENCAR,
BALB/cAnNCr, and C57BL/6NCr] were obtained from the National
Cancer Institute-Frederick Cancer Cancer Research Facility Animal
Resources Program and maintained as previously described (9). Five
breeding pairs of each of the following crosses were initiated: BALB/c
x SENCAR F, (hereafter called CSF,); SENCAR x BALB/c F, (here
after called SCF,); C57BL/6 x SENCAR F, (hereafter called B6SF,);
and SENCAR x C57BL/6 F, (hereafter called SB6F,). All breeding
pairs produced offspring with the exception of 3 of the 5 pairs in the
C57BL/6 x SENCAR cross. The mean size of 36 litters produced was
10.1 ±3.9 with a range of 3 to 19offspring. Coat colors of the offspring
were white for CSFi and SCFi mice and black or gray for B6SF, and
SB6Fi mice. FI offspring were used for experiments at 8 to 10 wk of
age, and dorsal hair was removed with electric clippers prior to irradia
tion. The appearance of the skin of the mice with pigmented hair was
similar to that of the albino mice. The small amount of residual hair
left after clipping was more visible in the pigmented mice. The hair
growth cycle was in the resting phase at treatment (8 to 10 wk), and
the growing phase began 1 to 2 wk later. Animals were routinely
monitored and found to be free of murine viruses, parasites, Myco-
plasma, and pathogenic bacteria.
UV Radiation. Mice were exposed to a bank of six FS40 sunlamps
(Westinghouse, Bloomfïeld,NJ) situated 20 cm above the animals.
During irradiation the animals were housed in wire-topped cages par
titioned into compartments for individual animals. The average fluence
rate at the position of the animals was 8.0 J/m2/s as measured by a
IL700 photometer with PT171C detector.
Persistent Hyperplasia and Tumor Induction. A total of 428 mice
from the parental strains and FI crosses (Table 1) were given a single
high dose (8.64 x IO4J/m2) of UV radiation which is known to cause
ulcération, persistent hyperplasia, and tumorigenesis in SENCAR mice
(16). All animals were inspected weekly, and gross skin reactions and
tumors were recorded. The incidence of persistent hyperplasia was
determined from the weekly observations at 4, 5, and 6 wk after
treatment, since the response was most prominent during this period.
Twenty-eight wk after irradiation the animals were sacrificed, and
samples of all skin tumors were taken for histopathological examina
tion. The probability of tumor development was determined by a life-
table analysis (17), and differences in tumor development between
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