Constancy
of Chromosome
Karyotype in Human Tumors
H.Ad. #1 and H.Ep. #3 Maintained in
Laboratory Animals*
HAROLDB. HALEY AND AGNES N. STROUD
(Department of Surgery, Stritch School of Medicine, Loyola University, Chicago; and Division of
Biological and Medical Research, Argonne National Laboratory, Argonne, Illinois)
SUMMARY
Two strains of human tumor H.Ep. #3 maintained in different laboratories were
studied for chromosome composition and compared with the chromosome analysis of
this tumor published by Levan in 1956. Chromosome patterns in both current strains
appeared to be similar to that previously described. This demonstrates considerable
stability through many animal passages.
Three strains of human tumor H.Ad. # 1 carried in different laboratories were also
studied. One strain had primarily 46 chromosomes of human type. The second
strain showed 61 per cent cells with 45 chromosomes, 13 per cent with 46, and 6 per
cent with 44. When 45 were present, the missing one was a member of pair 21 or 22.
With 44 chromosomes, a 21 or 22 and an X or 6 were missing. Rat cells (identified
by karyotype) were also seen in this tumor. The third strain (H.Ad. # 1 C) showed
equal numbers of cells with 45 and 46 chromosomes and an increased number of tetraploids.
It is suggested that these changes are due to conditions in the host animal encourag
ing stronger growth of the cells with 45 chromosomes and tetraploids.
Sequential studies of chromosome patterns in human
tumors in tissue culture have been reported (1, 8, 13).
Similar studies with in vivohuman tumors in experimental
animals over an extended period of time have been the
subject of preliminary reports by us and by others (4, 5,
18, 24). This communication is a full report of our work
in this area.
Conditioning of rats and hamsters with cortisone and
total-body irradiation has made it possible to maintain
permanently several human tumors in laboratory animals
(2, 21). Toolan first isolated human tumors H.Ep. #3
and H.Ad. #1 in 1953 and 1955, respectively (22, 23).
Since that time, these tumors have been maintained in heterologous hosts in her laboratory and by others. In differ
ent laboratories the growth characteristics of these tumors
have varied (24). This communication reports chromo
some studies on these two tumors to (a) discover whether
the behavior variation of these tumors in different labora
tories can be accounted for on the basis of chromosomal
changes and to (6) examine the chromosome karyotypes of
these human tumors which have been maintained in
heterologous hosts for more than 5 years. Our findings
in tumor H.Ep. # 3 will be compared with its chromosome
* This work was supported in part by American Cancer Society,
Grant T-120, and in part by the U.S. Atomic Energy Commission.
Received for publication September 13, 1963.
structure as reported by Levan in 1956 (10); chromosome
analysis of H.Ad. # 1 has not been previously published
(5).
Variation in growth-pattern behavior of these tumors in
different laboratories has been seen primarily in their ca
pacity to grow in normal unconditioned rats or hamsters.
In the original laboratory H.Ad. # 1 grew only in weanling
rats conditioned with total-body irradiation and cortisone
or in weanling hamsters treated with cortisone.1 In
Yohn's laboratory this tumor has been maintained for
more than 45 transplant generations in the cheek pouches
of normal untreated hamsters (24). In our laboratory
(HBH) the tumor is maintained in conditioned rats and
hamsters. When taken from a conditioned weanling rat
and transplanted subcutaneously as a cell suspension into
either 60- or 200-gm. normal, unconditioned rats, the tumor
will grow for 2 or 3 weeks as well as it grows in the condi
tioned rat. After this time regression takes place until,
in most animals, the tumor has completely regressed 4
weeks after implantation.
In the conditioned rat, al
though no further growth occurs after the 2- to 3-week
period, the tumor mass usually remains constant in size for
many months. If the tumor is taken after 2 weeks of
growth in the normal rat and transplanted to a second
generation of normal rat, tumor growth will occur. How; H. W. Toolan,
personal communication.
639
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
640
Cancer Research
ever, the tumor mass then is usually significantly smaller
than in the first generation. When this process is repeated
with transfer to a third generation, growth is insufficient to
allow subsequent passage. H.Ep. *3 behaves much like
H.Ad. jK1 in our laboratory (HBH) and has not grown in
normal animals in Toolan's laboratory.1 Such differences
in transplantation behavior could be due to changes hi the
tumor or to variations in immunologie mechanisms in
different strains or substrains of host animals.
MATERIALS AND METHODS
The basic structure of the H.Ad. $ 1 tumor consists of
small clusters of tumor cells enclosed in connective tissue.
The connective tissue is so firm that individual cells can
not be easily separated to provide satisfactory "squash"
preparations for chromosome analysis. Various combina
tions of trypsin-versene and hyaluronidase have been used
unsuccessfully. For purposes of these experiments, there
fore, although this tumor does not grow well intraperitoneally, preparations have been made as follows: H.Ad.
# 1 stock in our laboratory since 1958 (H.Ad. # 1 subline
A) is maintained in Wistar rats. A suspension of cells pre
pared from a stock tumor taken at 10-14 days of growth is
injected intraperitoneally into a weanling rat. At 3 or 4
days after injection the abdomen is opened, and the
peritoneal fluid containing tumor cells is aspirated for
chromosome preparations.
In 1961 the H.Ad. # 1 (subline B) was received by us again from Toolan's laboratory in
the strain of Wistar rats that she usually used. When the
tumor was of proper size, a similar cell suspension was
made. This was injected subcutaneously into conditioned
(21-23) Wistar rats to maintain the tumor line in our
laboratory. The same procedure was carried out so that
we could obtain peritoneal fluid containing loose tumor cells.
In November, 1962, we again received cortisone-dependent
H.Ad. $ 1 (subline C) from its parent laboratory, this time
in three rats shipped immediately after intraperitoneal
inoculation of tumor. On the 4th day after inoculation
chromosome preparations were made from one of these
rats.
The chromosome karyotypes of H.Ep. $ 3 were analyzed
in our laboratory 2 years after receiving this tumor from
Toolan (H.Ep. # 3 subline A) and also immediately after
receiving a second supply of animals bearing the tumor
(H.Ep. #3 subline B). The chromosome studies were
made directly on this tumor sent to us from the parent
laboratory, before passage in our own animals. Since
H.Ep. #3 contains less connective tissue, adequate
chromosome preparations can be made from subcutaneous
solid tumors.
The chromosome smear or squash technics used hi this
study are modifications of those of Moorhead et al. (12)
and of Hsu and Klatt (7). We found about 10-15 per cent
of the chromosomes spread at metaphase uncountable.
For this study 45 or more cells were scored in each subline.
RESULTS
H.Ep. # 8 tumor.—Levan reported in 1956 that H.Ep.
# 3 had a chromosome number of 69, with a range from 64
to 74 (10). The chromosomes were characteristic of a hu
man subtetraploid karyotype. He consistently found
Vol. 24, May 1964
i— —
i—T
rH.Ep.3BI
— —i—
—* —
1a
a—
,
CHROMOSOME
_l
NUMBER
CHART 1.—Chromosome number of H.Ep. #3 B showing a
modal number of 69. Cells in the range of chromosome number
40 are rat cells.
1-i
i-,B
r >
S'
1
S ¡SaSL^S3 ^H.Ep.SAa_a_
i
CHROMOSOME
1
r^V
4. a j.
i
NUMBER
CHART 2.—Chromosome number of H.Ep. #3 A showing a
modal number of 69 but with a wider range than in H.Ep. #3 B.
three or four satellite-bearing chromosomes which he felt
were sufficiently distinctive to be used as markers for this
tumor.
We examined metaphase chromosome spreads in 50 cells
for H.Ep. %3 as carried currently in Toolan's laboratory
(H.Ep. n 3 B) and in 45 cells for the tumor as carried by us
in rats and hamsters for 45 successive passages away from
Toolan's laboratory (H.Ep. #3 A). H.Ep. #3 B has es
sentially the same chromosome distribution as reported by
Levan 5 years ago (Chart 1). The marker satellites were
present as he described (Fig. 1). Modal chromosome num
ber was 69, with the cells showing an essentially human
karyotype. In the same tissue other cells were found with
42 chromosomes typical in karyotype of the rat. The tis
sue of origin of these rat cells was not obvious on morpho
logical grounds, although it might be assumed that they
arose from the rat stroma supporting the human tumor.
A few cells were seen with the tetraploid (138) number of
chromosomes.
Cytological analysis of H.Ep. H3 A showed the marker
satellites still present and the chromosome number of 69
maintained. However, the range is much wider than in
H.Ep. # 3 B, extending from 53 to 75 (Chart 2). Also seen
were rat cells, some human tetraploids, and a few cells
carrying 35 chromosomes.
The satellites noted by Levan (10) are evident in both
lines. These appear to be present on the larger acrocentric
chromosomes, particularly autosome pair 13 (4, 17).
Satellites are now recognized as being normally present on
the human chromosome pairs 13, 14, 15, 21, and 22, the
acrocentric chromosomes (3, 10, 16). H.Ep. #3, with the
triploid chromosome number of 69, has remained relatively
constant since its study by Levan. Karyotypic examina
tion of several cells demonstrates trisomy. Occurrence of
cells with approximately 138 chromosomes supports the
concept that the modal number of 69 is trisomal and not
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
HALEY AND STROUD—ChromosomeKaryotype in Human Tumors
641
colony-bred strains of Wistar rats, obtained from different
suppliers who had bred them separately over a period of
time, are likely to be genetically different. Presumably,
differences in host defense mechanisms are present.
COUNT4022411121427743213342449466634542616528134670371314301447212221482152226521721182218922*901369121924222*63TOTALNO.CELLSCOUNTED4710747
For the H.Ad. # 1 C subline received in 1962, chromo
somes were counted in only 47 cells from a tumor in one
animal that had been inoculated in Toolan's laboratory.
Fourteen cells (30 per cent) had 46 chromosomes; thirteen
(28 per cent) had 45 chromosomes; three (6 per cent) had
92 chromosomes; and six (13 per cent) had 90 chromo
somes. The 40 per cent of cells having 45 or 90 chromo
somes would seem to confirm that in the parent line there
has been an increase in the number of cells carrying 45
chromosomes as compared with the findings in the tumor
received by us in 1958.
TABLE 1
CHROMOSOME
DISTRIBUTIONIN THREE SUBLINES
OF TUMORH.AD. j*l
1SUBLINEA:Per
H.AD.
centNo.
cellsB:Per
centNo.
cellsC:Per
centNo.
cellsCHROMOSOME
* Exact chromosome number not certain.
random. Levan's study of this tumor apparently was one
of the earlier demonstrations of prominent consistent
satellites on human chromosomes.
H.Ad. #1 tumor.—H.Ad. # 1 has been maintained in
Toolan's laboratory since 1955. Chromosome studies of
this tumor have not been reported previously. The
karyotypes of the three sublines of H.Ad. # 1 are shown in
Table 1. Of 47 metaphase cells counted in H.Ad. # 1 A,
37 had 46 chromosomes, one had 43, four had 44, two had
45, and one had 47 chromosomes. Two cells were seen
with the tetraploid number of 92. The data show that
H.Ad. ft 1 A has a primary chromosome number of 46, with
a small spread around the mean. H.Ad. A1 B, on the
other hand, has a primary chromosome number of 45, with
a few at 43,44,46,47,92, and at scattered nonmodal counts
in the 112 metaphase cells scored in this tumor. The
chromosome complement, as far as arm ratios and lengths
are concerned, shows deviations of some pairs from the
Denver classification for the human karyotype (17). The
chromosome pairing may not be in agreement for this rea
son. Figure 2 is a karotype typical of these cells with 45
chromosomes. The missing chromosome is a small aerocentric, presumably from pair 21 or 22. An unpaired
chromosome is found which, from size and appearance, is
presumably an X or autosome 6 chromosome. An addi
tional elongated, unpaired chromosome is conspicuously
present in a number of cells. Identification is not made
of this chromosome. It is possible to speculate that its
additional chromatin material might represent a transloca
tion of the missing 21-22. Figure 3 is a karyotype typical
of cells with 44 chromosomes, the missing ones appearing
to be a 21 or 22 and the unpaired elongated chromosome.
The transplantation characteristics of H.Ad. # l B
appear somewhat different from those of H.Ad. # 1 A re
ceived in 1958 and maintained by us since then; the per
centage of "takes" is lower, and growth not so good in our
animals. However, the growth characteristics of H.Ad.
# 1 in Toolan's laboratory apparently are unchanged. It
must be emphasized that we are carrying the two strains of
H.Ad. $ 1 in Wistar rats from different sources. The two
DISCUSSION
The data reported herein should throw additional light
on questions of stemline stability of chromosome pattern
and changes occurring in specific lines over extended peri
ods of time. Many studies have been reported concerning
animal systems and human systems in tissue culture. It
is our purpose to integrate data from in vivo human tissues
with these data. The current concept that a specific
stemline is the dominant genome in a given tissue or cul
ture has been extensively discussed in a recent review by
Hsu (6). Many studies have indicated that the stemline
may change. This could result from mutational develop
ment of a new genome which, being stronger and more
vigorous, outgrows the original stemline. Another ex
planation is that, with multiple genomes present in a given
cell population, the frequency and growth vigor may be
determined by the specific environment. Conditions in
the environment may tend to stimulate the growth of one
genome and inhibit that of another. The systems which
we have studied are those involving heterologous trans
plantation—i.e., human tumors in passage through rats
and hamsters. Hsu comments on such systems as follows:
"Heterologous transplantation,
with cytotoxic antibodies
produced by the host, certainly represents an environment dras
tically different from that of the original. Only when frequent
transfers are made can a tumor line be maintained this way.
Selection of genomes from the population to fit the new environ
ment is, therefore, almost mandatory" (p. 126).
"Several conclusions can be drawn from these results: (1)
Different genomes have different metabolic requirements, (e) the
composition of a cell population can be molded according to the
environment given, and (3) once again, stemline is not a stable
entity" (p. 140).
These conclusions were drawn by Hsu from studies of
evolution in cell populations in tissue culture reported by
different authors. The studies he was referring to were
primarily of rodent tumors.
Sequential studies of chromosome constitution of human
tumors in tissue culture have been reported recently.
Auersperg et al. reported three cell cultures derived from
carcinomas of the human cervix (1). Modal numbers of
chromosomes were 45, 51, and 120-130. The 45-chromosome line had two extra chromosomes and three absent
chromosomes. Ishihara et al. reported nine long-term
cultures of cells from human tumors (8). The modes were
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
642
Vol. 24, May 1964
Cancer Research
all near-triploid, ranging from 66 to 75, with a considerable
spread. Most of their cell lines demonstrated new mark
ers. They state :
"It is interesting to note that the chromosome number, mode,
and constitution remained fairly stable in each culture line during
the period of study. Thus, a line characterized by 'new' marker
chromosomes retained these markers on subsequent subculturing
(in some, over 70 generation passages in 3 years). The retention
of this individuality
in the chromosomal constitution
possibly
indicates that the cell line has originated from different somatic
karyotypes, most of which may have been malignant.
This is
all the more apparent from repeated observations that cultured
normal tissue may retain its diploid characteristics
for long
periods" (p. 378).
Further, they stated :
"It is possible that our in vitro conditions favored the growth
of cells with a near-triploid number of chromosomes, be they of
normal or malignant origin" (p. 379).
Norryd et al. report chromosome studies of tissue-culture
cells of human tumor H.Ep. # 2, which had also been previ
ously studied by Levan (10, 13). Currently this line
shows a hypertriploid stemline of 77 chromosomes, with a
range of 69-81. Three marker chromosomes are present.
Nowell and Hungerford reported one patient with a modal
number of 45 in bone marrow and in peripheral blood
grown in normal plasma and with a modal number of 46 in
peripheral blood grown in autologous plasma (14).
In vivo studies of chromosome patterns in heterologous
rodent transplantation have been reported by various
workers, including Ising (9) and one of us (ANS) (19, 20).
These studies, on Krebs-2 and Ehrlich mouse ascites
carcinomas in rats, showed reduction in chromosome num
bers and alterations in karyotypes which they attributed to
changes in host environment.
Our studies with H.Ep. # 3 were performed 5 years and
more than 250 transplant generations later than the study
reported by Levan in 1956 (10). In addition, the line re
ferred to as H.Ep. # 3 A was carried for 2 years away from
the parent laboratory in different substrains of both rats
and hamsters and was handled by different technicians
with some changes in method. It would seem remarkable
that after this experience the stemline number would
appear to be the same as previously reported and that the
only evident change would be a somewhat wider range of
chromosome numbers. The persistence of the chromo
some markers would seem consistent with the tissue-culture
reports previously cited. Ishihara's and Norryd's culture
lines in the near-triploid range and the persistent triploid
number in H.Ep. # 3 again point up the question as to what
environmental conditions have encouraged the triploid
rather than diploid growth (8, 13).
Another speculation raised is the presence of the prom
inent satellites. Since satellites have been reported on all
ten human acrocentric chromosomes, the possibility is
suggested that the original tumor in the patient or the
patient's normal karyotype may have included these
prominent satellites.
Interpretation of our experiences with H.Ad. # 1 is some
what difficult. Of primary importance is the demonstra
tion that this tumor, which was removed from a human
patient in 1955, after serial transplantation in rodents
every 2 weeks, still has a close-to-normal human chromo
some number and karyotype 7 years later. A recent paper
reports similar findings with human tumor H.S. #1, which
after many years' passage in rats and hamsters maintains
a chromosome count close to 46 (18). These studies dem
onstrate that human diploid chromosomes apparently can
be maintained by in vivo passage. The slight variations
in chromosome number and karyotype in the different
sublines would seem to suggest that, since both 45- and
46-chromosome stemlines appear to be present, environ
mental conditions may determine which stemline grows
best. It is, of course, impossible to define those differences
in conditions responsible for the difference between the
sublines. One would strongly suspect that the different
substrains of host animals would be a likely source of such
differing environments.
All tumors examined had cells with tetraploid numbers
of chromosomes, subline H.Ad. I C showing increased num
bers of these cells. In several preparations, cells with hu
man chromosomes and other cells with 42 typical rat
chromosomes were seen. The intermingling of rat and
human cells is of interest. A few of the human cells also
had 42 chromosomes. Differentiation between the two was
made by karyotype identifications. Cells with 35 chro
mosomes were frequently found in metaphase spreads from
various tumors. Their cellular origin could not be deter
mined from their karyotype, so this remains an unex
plained observation.
ACKNOWLEDGMENTS
We are grateful to Beverly
technical assistance.
R. Svoboda
for her competent
FIG. 1.—Metaphase spread of a H.Ep. jj(3 tumor cell showing
some of the prominent satellites observed previously by Levan.
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
•
G43
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
FIG. 2.—An idiogram of H.Ad. # l B celj with 45 chromosomes.
Missing is a small acrocentric chromosome from pairs 21-22. The
unidentified elongated chromosome is evident.
FIG. 3.—An idiogram of H.Ad. # l B cell with 44 chromosomes.
A small acrocentric chromosome from pairs 21 to 22 and the
elongated chromosome are both missing.
644
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
(ÃŽ
ff 1C\\ x
ri if H ri n \\
123
456
II
O il
la
i i
i « il
k_
13
19
14
20
15
16
2l
II
12
ii
tt
17
r
22
fil
ri Jt H <ri«i
« it
13
IX
19
14
ti idi
15
16
. ..
II
A _
20
12
2l
ft
«i
17
18
IL
22
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
HALEY AND STROUD—Chromosome
Karyotype in Human Tumors
REFERENCES
1. AUEESPEBG,N., ANDHAWRYLUK,A. P. Chromosome Observa
tions on Three Epithelial-Cell
Cultures Derived from Carci
nomas of the Human Cervix. J. Nati. Cancer Inst., 28:605-28,
1962.
2. CHUTE, R. N.; SOMMERS,S. C.; ANDWARBEN,S. Heterotrans
plantation
of Human Cancer. II. Hamster Cheek Pouch.
Cancer Res., 12:912-14, 1952.
3. COOPER, H. L. II. The Use of Human Chromosome Markers in
Linkage Studies. Trans. N.Y. Acad. Sci., 24:383-94, 1962.
4. HALEY, H. B.; STROUD,A. N.; ANDSVOBODA,B. R. Studies of
Human Tumor Karyotypes
during Heterotransplantation.
Proc. Am. Assoc. Cancer Res., 3:232, 1961.
5. HALEY, H. B.; WELLBAND, W. A.; SVOBODA,B. R.; AND
STROUD, A. N. Relationships between Chromosomes and Bio
logical Behavior of Two Strains of Transplantable
Human
Tumor H.Ad. 1. Surg. Forum, 8:115-17, 1962.
6. Hsu, T. C. Chromosomal Evolution in Cell Populations. Int.
Rev. Cytol., 12:69-161, 1961.
7. Hsu, T. C., AND KLATT, O. Mammalian Chromosomes in
Vitro. IX. On Genetic Polymorphism in Cell Populations. J.
Nati. Cancer Inst., 21:437-73, 1957.
8. ISHIHARA, T.; MOORE, G. E.; AND SANDBERG,A. A. The in
Vitro Chromosome Constitution of Cells from Human Tumors.
Cancer Res., 22:375-79, 1962.
9. ISING, U. Chromosomal Changes in Ehrlich's Mouse Ascites
Cancer on Repeated Transfer through Hamsters and Rats.
Acta Path. Microbiol. Scandinav., 40:315-27, 1957.
10. LEVAN, A. Chromosome Studies on Some Human Tumors and
Tissues of Normal Origin Grown in Vivo and in Vitro at the
Sloan-Kettering Institute. Cancer, 9:648-63, 1956.
11. MILLER, O. J.; MUKHERJEE, B. B.; ANDBERG, W. R. Normal
Variations in the Human Karyotype. Trans. N.Y. Acad. Sci.,
24:372-82, 1962.
12. MOORHEAD,P. S.; NOWELL, P. C.; MELLMAN,W. J.; BATTYRS,
D. M.; ANDHUNGERFORD,D. A. Chromosome Preparations of
Leukocytes Cultured from Human Peripheral Blood. Exp.
Cell Res., 20:613-16, 1960.
647
13. NORRYD,C., ANDFjELDE, A. The Chromosomes in the Human
Cancer Cell Tissue Culture Line H.Ep. #2. Cancer Res., 23:
197-200, 1963.
14. NOWELL,P. C., ANDHUNGERFORD,D. A. Chromosome Studies
in Human Leukemia. IV. Myeloproliferative
Syndrome and
Other Atypical Myeloid Disorders. J. Nati. Cancer Inst., 29:
911-31, 1962.
15. OHNO,S. More About the Mammalian X Chromosome. Lancet,
pp. 152-53. July 21, 1962.
16. OHNO, S.; TRUJILLO, J. M.; KAPLAN, W. D.; ANDKINOSITA, R.
Nucleolus-Organisers
in the Causation
of Chromosome
Anomalies in Man. Lancet, pp. 123-26. July 15, 1961.
17. A Proposed Standard System of Nomenclature
of Human
Mitotic Chromosomes. Lancet, pp. 1063-65. May 14, 1960.
18. RUTISHAUSER,A., ANDHAEMMERLi,G. W. Karotypen transplantabler menschlicher Tumorzellen. In: Cytogenetik transplantabler tierischer
und menschlicher
Tumoren,
p. 31.
Zurich: Kommissions Verlag Leeman A. G., 1963.
19. STROUD, A. N.; BRUES, A. M.; CHATTERLEY, D. H.; AND
SUMMERS,M. Serial Transplantation
of Krebs-2 and Ehrlich
Ascites Tumors to Rats. Cancer Res., 17:1102-7, 1957.
20. STROUD,A. N.; BRUES, A. M.; ANDSVOBODA,B. R. Change in
Chromosome Number of Krebs-2 Mouse Ascites Carcinoma
during Heterologous Growth. Proc. Am. Assoc. Cancer Res.,
3:153, 1960.
21. TOOLAN, H. W. Growth of Human Tumors in Cortisonetreated Laboratory Animals. Cancer Res., 13:389-94, 1953.
22.
. Transplantable
Human Neoplasms Maintained
in
Cortisone-treated
Laboratory Animals: H.S. Al; H.Ep. #1;
H.Ep. *2; H.Ep. «3; and H.Emb.Rh.
#1. Ibid. 14:660-66,
1954.
23.
. Permanently Transplantable
Human Tumors Main
tained in Conditioned Heterologous
Hosts: H.Chon.
ml,
H.Ep. #4, and H.Ad. #1. Ibid., 17:418-20, 1957.
24. YOHN, D. S.; HAMMON,W. M.; ATCHISON,R. W.JAND CASTO,
B. C. Serial Heterotransplantation
of Human Adenocarcinoma
#1 in the Cheek Pouch of Unconditioned Adult Syrian Ham
sters. Cancer Res., 22:443-48, 1962.
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.
Constancy of Chromosome Karyotype in Human Tumors H.Ad.
#1 and H.Ep. #3 Maintained in Laboratory Animals
Harold B. Haley and Agnes N. Stroud
Cancer Res 1964;24:639-647.
Updated version
E-mail alerts
Reprints and
Subscriptions
Permissions
Access the most recent version of this article at:
http://cancerres.aacrjournals.org/content/24/4_Part_1/639
Sign up to receive free email-alerts related to this article or journal.
To order reprints of this article or to subscribe to the journal, contact the AACR Publications
Department at [email protected].
To request permission to re-use all or part of this article, contact the AACR Publications
Department at [email protected].
Downloaded from cancerres.aacrjournals.org on June 16, 2017. © 1964 American Association for Cancer Research.