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From the Department of Pathology,*
the James Buchanan
Brady Urological Institute,
and the Johns
Hopkins Oncology Center,
The Johns Hopkins
University Medical Institutions, Baltimore, Maryland
Proliferation in the setting of longstanding chronic inflammation
appears to predispose to carcinoma in the liver, large
bowel, urinary bladder, and gastric mucosa. Focal
prostatic atrophy, which is associated with chronic
inflammation, is highly proliferative (Ruska et al,
Am J Surg Pathol 1998, 22:1073–1077); thus the focus of
this study was to more fully characterize the phenotype of the atrophic
cells to assess the feasibility of the proposal that they may be
targets of neoplastic transformation. The 
-class glutathione
S-transferase (GSTP1), a carcinogen-detoxifying
enzyme, is not expressed in >90% of prostate carcinomas
(CaPs). GSTP1 promoter hypermethylation, which
appears to permanently silence transcription, is the most
frequently detected genomic alteration in CaP (Lee et al, Proc
Natl Acad Sci USA 1994, 91:11733–11737; >90% of cases). In
high-grade prostatic intraepithelial neoplasia (PIN), this
alteration is present in at least 70% of cases (Brooks et al,
Cancer Epidemiol Biomarkers Prev, 1998, 7:531–536).
Although normal-appearing prostate secretory cells rarely express
GSTP1, they remain capable of expression, inasmuch as
GSTP1 promoter hypermethylation is not detected in
normal prostate. Fifty-five lesions from paraffin-embedded
prostatectomy specimens (n = 42) were stained for
GSTP1, using immunohistochemistry. Adjacent sections were
stained for p27Kip1, Ki-67, androgen
receptor (AR), prostate-specific antigen (PSA),
prostate-specific acid phosphatase (PSAP), Bcl-2, and
basal cell-specific cytokeratins (34ßE12). With normal prostate
epithelium as the internal standard, staining was scored for
each marker in the atrophic epithelium. The lesions showed two cell
types, basal cells staining positive for 34ßE12, and
atrophic secretory-type cells staining weakly negative for 34ßE12.
All lesions showed elevated levels of Bcl-2 in many of the
secretory-type cells. All lesions had an elevated staining index for
the proliferation marker Ki-67 in the secretory layer and decreased
expression of p27Kip1, a finding reminiscent of
high-grade PIN (De Marzo et al, Am J Pathol 1998,
153:911–919). Consistent with partial secretory cell
differentiation, the luminal cells showed weak to moderate
staining for androgen receptor and the secretory proteins PSA and PSAP.
All atrophic lesions showed elevated GSTP1 expression in many of the
luminal secretory-type cells. Because all lesions are
hyperproliferative, are associated with inflammation,
and have the distinct morphological appearance recognized as prostatic
atrophy, we suggest the term "proliferative inflammatory
atrophy" (PIA). Elevated levels of GSTP1 may reflect its inducible
nature in secretory cells, possibly in response to increased
electrophile or oxidant stress. Elevated Bcl-2 expression may be
responsible for the very low apoptotic rate in PIA and is
consistent with the conclusion that PIA is a regenerative lesion. We
discuss our proposal to integrate the atrophy and high-grade
PIN hypotheses of prostate carcinogenesis by suggesting that
atrophy may give rise to carcinoma either directly, as
previously postulated, or indirectly by first developing into
high-grade PIN.
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