Loss of Retinoblastoma Protein Expression
is Frequent in Small Cell Neuroendocrine
Carcinoma of the Cervix and
is Unrelated to HPV Type
C, SIMON HERRINGTON, MBBS, MRCPATH, DPHBL,
DAVID GRAHAM, MSc, SHIRLEYA, SOUTHERN, FIMLS,
ASHWIN BRAMDEV, MBCHB, FFPATH (SA),
AND RUN JAN CHETrY, MB BCH, FRC PATH (UK), DPHIL
We have previously identified an inverse relationship between
p53 and refinoblastoma protein (pRb) immunoreactivity in non-small
cell carcinoma of the cervix. Because pRb is infrequently expressed in
small cell carcinoma of the lung, we analyzed 25 small cell neuroendo-
crine carcinomas of the cervix to test the hypotheses that 1) lack of
pRb expression is associated with the neuroendocrine phenotype in
human papillomavirus (HPV)-associated cervical carcinoma and 2)
the inverse relationship between p53 and pRb immunoreactivity also
occurs in these tumors. I-IPV type was analyzed by PCR, HPV
distribution by in situ hybridization and expression of p53 and pRb by
immunohistochemistry. All of the tumors contained HPV sequences,
with 13 tumors HPV 16 positive, 11 HPV 18 positive, and 1 HPV45
positive. In situ hybridization showed large intranuclear dot-like
signals in all positive tumors, suggesting viral integration. No multiple
infections were identified. Expression of retinoblastoma protein was
not detectable in 23 tumors (92%), the remaining two showing only
weak, focal expression. Expression of p53 protein was variable in
dislribution and intensity. It did not correlate with HPV type, and
there was no relationship with pRb immunoreactivity. These data
indicate that, although there is no reciprocal relationship between p53
and pRb immunoreactivity in these tumors, refinoblastoma protein is
infrequently expressed in HPV-containing small cell neuroendocrine
carcinoma of the cervix, irrespective of infecting HPV type. This is
consistent with the reported findings in small cell carcinoma of the
lung and suggests that the small cell neuroendocrine phenotype may
be related to the abrogation of retinoblastoma protein function. HuM
PATrIOL30:906-910. Copyright © 1999 by W.B. Saunders Company
Key words: papillomavirus, small cell carcinoma, p53, retinoblas-
toma.
Abbreviatim~: HPV, human papillomavirns; pRb, refinoblastoma
protein; PCR, polymerase chain reaction.
Human papillomaviruses (HPV) infection is the
major causative factor in cervical carcinogenesis, 1 with
epidemiological evidence indicating that most cervical
neoplasia is attributable to HPV. 2 More than 95 HPV
types have been described, and phylogenetic analysis
has identified 11 separate groups of anogenital HPVs
based on their sequence homology? Analysis of clinical
lesions has identified low-risk, intermediate-risk, and
high-risk HPV types4 based on their relative risk associa-
tions with intraepithelial and invasive squamous lesions.
HPV 18 is associated particularly with invasive disease,
and it has been suggested that tumors containing this
viral type are more aggressive than those containing
other HPV types. 5This is supported by the fact that HPV
18 is found in clinically aggressive tumor types, such as
clear cell adenosquamous carcinoma6 and small cell
carcinoma,v
The suggestion that the neuroendocrine pheno-
From the University of Liverpool, Department of Pathology,
Royal Liverpool University Hospital, Liverpool, United Kingdom; and
the Department of Pathology, University of Natal School of Medicine,
Durban, South Africa. Accepted for publication March 29, 1999.
Supported by the Universities of Liverpool and Natal.
Address correspondence and reprint requests to C.S. Herring-
ton, University of Liverpool, Department of Pathology, Duncan
Building, Royal Liverpool University Hospital, Liverpool L69 3GA,
United Kingdom.
Copyright © 1999 by W.B. Saunders Company
0046-8177/99/3008-0005510.00/0
type of small cell neuroendocrine carcinoma of the
cervix is associated with infection with HPV 188 is of
potential biological significance. The protein products
of the early genes of HPVs are capable of binding to and
inactivating cell cycle control proteins, particularly p53
and the retinoblastoma protein (pRb) which bind to
the E6 and E7 proteins, respectively. 9 The binding orE7
to pRb leads to abrogation of the G1/S control point
and allows cells to pass directly through the restriction
point into late G1 phase without a requirement for
cyclin D1 expression. 1° No clear difference has been
identified between the ability of HPV 16 and 18 gene
products to abrogate this checkpoint. However, HPV 18
integrates more frequently into the host genome, 11 and
therefore the aggressive behavior of these tumors may
be related to early integration events with consequent
upregulation of HPV early gene transcription and
abrogation of p53 and pRb function.
This suggestion is supported by reports that small
cell carcinomas of the lung express pRb infrequently.12,1s
However, it is not known whether this absence of pRb
expression is common to small cell neuroendocrine
carcinomas in other anatomic sites, including the cer-
vix. We have previously identified pRb expression in
most (86%) squamous cell carcinomas of the cervix and
also showed an inverse relationship between p53 and
pRb immunoreactivity. 14 In view of these observations,
we analyzed a series of small cell neuroendocrine
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