[CANCER RESEARCH 50, 438-443. January 15, 1990]
Presence of Villin, a Tissue-specific Cytoskeletal Protein, in Sera of Patients and an
Initial Clinical Evaluation of Its Value for the Diagnosis and Follow-up of
Colorectal Cancers1
B. Dudouet, L. Jacob, P. Beuzeboc, H. Magdelenat, S. Robine, Y. Chapuis, B. Christoforov, G. A. Cremer,
P. Pmiillanl, P. Bonnichon, F. Pinon, R. J. Salmon, A. Pointereau-Bellanger, J. Bellanger, M. T. Maunoury,
and D. Louvard2
Département de Médecineinterne [L. J., B. C., G.A. C.J, Clinique Chirurgicale [Y. C., P. Bo.J, and Poste de Transfusion sanguine ¡F. P.], Hôpital Cochin, 27, rue du
Faubourg Saint Jacques, 75674 Paris Cedex 14; Département de Médecineoncologique [P. Be., P. P.],Laboratoire de radiopathologie ¡H.M.], and Service de Chirurgie
[R. J. S.], Institut Curie, 26 rue d'Ulm, 75005 Paris; Service de Gastroenterologie, Pr. Y. Le Quintrec, Hôpital Rothschild, 75012 Paris [J. B.]; Pharmacie Hôpital
Salpétriére, 83 bd de l'Hôpital, 75013 Paris [A. P. B.]; Institut Gustave Roussy, 39 rue Camille Desmoulins, 94805 Villejuif Cedex [M. T. M.J; and Unité de Biologie
des Membranes, Département de Biologie Moléculaire, Institut Pasteur, 25 rue du Docteur Roux, 75724 Paris Cedex 15 [B. D., S. R., D. L.], France
ABSTRACT
Villin is an actin-binding protein found in a few normal adult epithelia,
namely epithelial cells in the digestive and urogenital tracts. Moreover,
villin production is maintained in malignant cells. We assumed that cell
lysis and necrosis of solid tumors producing villin might result in villin
release into blood. We analyzed the villin content of sera from 788
patients and controls using an enzyme-linked immunosorbent assay.
Patients and controls were classified into healthy donors, patients with
benign diseases of the gastrointestinal tract, patients with colorectal
cancers, and patients with malignant nondigestive diseases. In the panel
of sera analyzed, the sensitivity of the assay for colorectal cancers was
50.5%, and its overall specificity for malignant digestive tumors was
94.5%. Results were statistically analyzed comparing each group of sera
with each other. We conclude that the presence of villin is indicative of
a pathological state in the gastrointestinal tract (/' < 0.001). Finally, we
followed villin levels after tumor resections (60 patients). We found that
the villin level in sera remains low in remissions but is raised in recur
rences.
We suggest that the villin assay may have clinical utility as a diagnostic
adjunct for adenocarcinoma of the gastrointestinal tract. It may also have
some value in monitoring patients with advancing colorectal carcinomas
after resection of these tumors.
INTRODUCTION
Enterocytes, the epithelial cells of the intestinal mucosa,
exhibit a functional and morphological polarity. Their apical
plasma membrane shows an ordered array of microvilli forming
the brush border. Each microvillus is supported by a cytoskel-
eton based on actin microfilaments. These actin microfilament
bundles are associated with a few actin-binding proteins (1).
Among them, villin, a M, 95,000 protein, is able to bind actin
in a calcium-dependent process. Production of villin and its
regulation were previously studied in our laboratory in vivo and
in cell cultures (2-4). During ontogenesis of the human diges
tive tract, villin is found in immature intestinal cells as early as
the eight wk of gestation of the human fetus, before the final
stages of histogenesis. Similarly, villin is found in adult undif-
ferentiated crypt cells of the intestinal mucosa. In the adult
human, high levels of villin were primarily found in epithelial
cells with a well-organized brush border, namely the epithelial
cells in the small and large intestine and in cells lining the
proximal tubules of the kidney.
Received 2/27/89; revised 7/13/89; accepted 9/25/89.
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.
1This work was supported by grants from the Institut National de la Santé et
de la Recherche Médicale (No. 86-7008), by the Fondation pour la Recherche
MédicaleFrançaise,by the Association pour la Recherche sur le Cancer (No.
6379), théCNRS (UA-1149), and thé Ligue Nationale Françaisecontre leCancer.
1To whom requests for reprints should be addressed.
This restricted tissue specificity of villin is also conserved
during neoplasie processes. In this respect, it is particularly
worth recalling that villin continues to be produced in colorectal
tumors at all stages of epithelial cell transformation, but that
villin is conspicuously absent from tumors arising from cell
types in which it is not normally found (5, 6).
These observations are in contrast with the more generalized
production of CEA,3 a tumor marker that is routinely assayed
for screening and follow-up of patients with tumors of the
digestive tract. For example, it is now well established that
CEA is found in several normal cells of numerous origins (7-
9).
The above mentioned properties of villin prompted us to
determine whether it is released into the blood circulation, due
to lysis of malignant cells or by means of another unknown
mechanism, which could indicate the existence of a lesion in
the digestive tract. We therefore investigated the presence of
villin in the sera of 788 patients and controls with an ELISA
developed for this study in our laboratory. Our initial data
showed that the occurrence of villin in human sera corre
sponded to the pathological state of the gastrointestinal tract.
Moreover, the presence of villin in sera was very often associ
ated with a malignant digestive tumor. This is the first report
of the presence of villin in human sera. We discuss the value of
villin as a diagnostic adjunct for the diagnosis and follow-up of
patients with colorectal carcinomas.
MATERIALS AND METHODS
Clinical Specimens. Age- and sex-matched healthy controls were
provided by a serum bank from the Centre National de Transfusion
sanguine (HôpitalCochin, Paris, France). The mean age of these donors
was 37 ±15 yr. They included a roughly equal proportion of men and
women. The mean age of donors from whom sera contained detectable
amounts of villin was 39 ±11yr. Coded serum collections from patients
bearing gastrointestinal tumors, adenocarcinoma of other organs, or
benign diseases were obtained from three hospitals (Departments of
Internal Médecineand Surgery). For this study, the diagnosis and
follow-up of patients bearing digestive tumors were carried out with
routine clinical and endoscopie examinations. All specimens (healthy
donors' sera, benign and malignant disease patients' sera) were coded
and collected during the same period of time. All of them were aliquoted
and stored in the same conditions at —¿20°C. We have observed that
villin is stable in these storage conditions. Provided that the assay was
performed on frozen and thawed samples, there was no significant
variation in the measured villin concentration. Medical histories of
patients were checked to validate this information and to secure addi
tional data about the serum withdrawal date and about the ultimate
3The abbreviations used are: CEA, carcinocmbryonic antigen; ELISA, enzyme-
linked immunosorbent assay; PBS, phosphate-buffered saline; BSA, bovine serum
albumin.
438
Research.
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