[CANCER RESEARCH 54, 4532-4538, Augusl 15, 19<M|
Integrins and Laminins in Human Renal Carcinoma Cells and Tumors
Grown in Nude Mice1
Matti Korhonen,2 Hannu Sariola, Victor E. Gould, Lauri Kangas, and Ismo Virtanen
Department of Anatomy. P. O. Box 9 ¡M.K., I. V.¡,Department of Pathology, P. O. Box 21 IH. S.¡,and Institute of Biotechnology, P. O. Box 45a ¡H.S.¡,FIN-(Xmi4 University
nf Helsinki, Helsinki, and Orion Corporation, Farmos Research, P. O. Box 425, FIN-20101 Turku ¡L. K.], Finland, and Department of Pathology, Rush Medical College,
Chicago, Illinois 606/2 ¡V.E. G.J
ABSTRACT
We studied by indirect immunofluorescence microscopy the distribu
tion of integrins and laminins in four human renal cell carcinoma cell lines
(CAKI-2, A498, CAKI-1, and ACHN) in vitro and in s.c. xenografts in
nude mice. In vitro, all four cell lines expressed the a,, <i„ a,., /ÃOE,, |>,. and
/!, subunil.s and three expressed the <>,,subunit; all cell lines expressed
laminili A, Bl, and B2 chains.
Histologically, the CAKI-2 and A498 cells formed differentiated grade
1 (Gl) and C,2 tumors, respectively, while the CAKI-1 and ACHN cells
formed poorly differentiated (..* tumors. The described integrin profile
was largely retained upon xenografting. Basal polarization of the <>,and
«,,integrin subunits was found in the differentiated tumors, and human
laminins were detected as discrete linear structures surrounding tumor
cell clusters in these tumors, suggesting that the cells have retained a
polarized cell-laminin interaction characteristic of normal tubular epithe
lial cells. A disorganized distribution of ¡ntegrinsand laminins was noted
in the G3 tumors.
We conclude that these renal carcinoma cell lines displayed an integrin
repertoire similar to that of clinical renal carcinomas and retained it upon
xenografting. Furthermore, the organization of integrins and laminins in
the xenografts correlated with histológica! grade.
INTRODUCTION
Interactions of cells with the ECM3 are important determinants of
tissue morphogenesis and of cell differentiation (1, 2), alterations in
these processes may explain certain aspects of malignant cell behavior
(3). Laminins (4) have a role in the physical architecture of BMs and
may also be important providers of differentiational cues to epithelial
cells as was shown in the kidney (5, 6). Furthermore, degradation and
disorganization of BMs seem to correlate with invasive characteristics
of tumors (7).
Integrins are a family of heterodimeric transmembrane receptors con
sisting of an a and a ß subunit that mediate binding of cells to the ECM
and to other cells (8). Our studies (9, 10), confirmed by others (11-14),
revealed that different integrins are expressed in specific nephron seg
ments in the developing and adult human kidney. Further studies on
human RCC suggested that increased expression of the av and decreased
expression of the a6 subunits correlate with increasing histological grade
of human RCCs (15). Furthermore, the more anaplastic RCC tumors
showed a reduction of organized cell-BM interactions.
In this study, we attempted to develop a model wherein changes in
integrin expression could be correlated with the behavior of the RCC
cells. For this purpose, we characterized the integrin expression pro
files of four human RCC cell lines and corresponding xenografts in
nude mice. Using antibodies mostly specific to human proteins, we
Received 3/11W; accepted 6/9/94.
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
18 U.S.C. Section 1734 solely to indicate this fact.
1 This work was supported by a research contract with the Finnish Medical Research
Council and grants from the University of Helsinki, the Finnish Medical Society "Duo-
decim." the Ida Montin Foundation, and the Research and Science Foundation of Farmos.
; To whom requests for reprints should be addressed.
•' The abbreviations used are: ECM. extracellular matrix; BM. basement membrane;
MAb, monoclonal antibody: RCC. renal cell carcinoma: GSA-I-B4, Griffonia simplici-
folia agglutinin 1-B4; FITC, fluorescein isothiocyanate.
studied the distribution of integrins and laminin chains in the tumors.
We found that integrin expression of RCC cells remains largely
unchanged upon xenografting. Significantly, the four cell lines pro
duced tumors differing in their degree of differentiation, which cor
related with integrin and laminin organization within the tumors.
MATERIALS AND METHODS
Immunohistochemistry. Integrin subunits were detected using MAhs:
TS2/7 [anti-a, (16)]; 10G11 (anti-a,; CLB, Central Laboratory of the Neth
erlands Red Cross Blood Transfusion Service, Amsterdam, the Netherlands);
J143 [anti-a, (17, 18)]; P4G9 (anti-a4; Gibco BRL, Gaithersburg, MD); BIE5
[anti-a, (19)]; P1D6 (anti-a.,; Gibco BRL); GoH3 (anti-ah; CLB); LM142.69
[anti-a,. (20)]; 102DF5 [anti-ß, (21)]; 90BB10 [anti-ß, (22)]; AA3 [anti-ß
(23)]; and IA9 [anti-ß,(24)].
MAbs to detect the laminin chains were; 4C7. A chain; 4E10, Bl chain; and
2E8, B2 chain (Ref. 25; Gibco BRL). Rabbit anti-laminin serum (26) was used
in some double labeling experiments.
The MAb PKK1 against cytokeratins 8, 18, and 19 (27) and an anti-
cytokeratin 19 serum (28) were used to identify carcinoma cells within the
tumors; GSA-I-B4 was used to identify mouse endothelial cells (29). In some
double labelings. the 4.6-diamidino-2-phenylindole fluorochrome (bisbenzim-
ide H 33258 fluorochrome; Riedel-De Haen AG, Seelze-Hannover, Germany)
was used to reveal nuclei. An antiserum to vinculin (raised against protein
purified from chicken gizzard as described earlier (30)] was used to identify
focal contacts in cultured cells.
For screening the cell lines for the expression of integrins and laminins, the
cells were seeded on coverslips and allowed to attach and spread overnight in
the presence of serum. Five-/j.m cryosections and cultured cells were processed
for immunostaining as described previously (9, 21). The following fluoro-
chrome-coupled secondary antibodies were used: FITC-conjugated goat anti-
mouse IgG serum (Jackson Immunoresearch Laboratories, West Grove, PA);
tetramethylrhodamine fluorescein isothiocyanate-coupled sheep anti-mouse
IgG serum (Cappel, Organon Teknika, West Chester, PA); FITC-goat anti-rat
IgG serum (minimal cross-reaction to mouse IgG; Jackson); tetramethylrho
damine fluorescein isothiocyanate-goat anti-rabbit IgG serum (Jackson);
FITC-goat anti-rabbit IgG (Jackson). Negative controls were performed by
applying the mere secondary antibodies to the sections or cells, revealing
frequent artifactual reactivity in the necrotic areas of the tumors. The anti-
mouse secondary antibodies revealed reactivity in the stroma of the tumors,
apparently due to endogenous mouse immunoglobulins. In these cases we
carried out careful controls with mere secondary antibodies or double immu-
nostainings with anti-cytokeratin serum and staining serial sections with the
MAh PKK1 in order to identify the carcinoma cells.
To evaluate whether the integrin and laminin MAbs would recognize the
corresponding mouse proteins, we exposed sections of normal mouse kidney
and skin to the various antibodies and compared the results with controls
obtained with secondary antibodies. We found that, except for GoH3 [anti-a,,
(30)], the MAbs are specific for human proteins. Carcinoma cell-associated a,,
immunoreactivity was identified by double immunostainings of the sections
with anti-cytokeratin 19 serum or staining serial sections with the MAb PKK1.
Cell Lines, Nude Mice, and Tumors. Four human RCC cell lines were
used in the study: A498, isolated from a primary renal carcinoma; CAKI-1,
isolated from a cutaneous metastasis of a renal adenocarcinoma; CAKI-2,
isolated from a renal adenocarcinoma; and ACHN, isolated from malignant
pleural effusion of a patient with widely metastatic renal adenocarcinoma
(Refs. 32-35; American Type Culture Collection, Rockville, MD). The his
tology of the original tumors is not known. The cells were grown in RPMI
4532
on March 2, 2016. © 1994 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from