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Preferential Loss of Fhit Expression in Signet-Ring Cell and Krukenberg

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Preferential Loss of Fhit Expression in Signet-Ring Cell and Krukenberg 0023-6837/02/8209-1201$03.00/0 LABORATORY INVESTIGATION Vol. 82, No. 9, p. 1201, 2002 Copyright © 2002 by The United States and Canadian Academy of Pathology, Inc. Printed in U.S.A. Preferential Loss of Fhit Expression in Signet-Ring Cell and Krukenberg Subtypes of Gastric Cancer Yu-Ting Chang, Ming-Shiang Wu, Chee-Jen Chang, Pei-Hsin Huang, Su-Ming Hsu, and Jaw-Town Lin Departments of Internal Medicine (Y-TC, M-SW, J-TL) and Pathology (P-HH, S-MH), National Taiwan University Hospital, and Department of Clinical Research (C-JC), College of Medicine, National Taiwan University, Taipei, Taiwan SUMMARY: Gastric cancer of youth is predominantly a disease of women, usually of the signet-ring cell subtype, with a predilection for metastasizing to the ovaries. The metastatic ovarian tumor is named a Krukenberg tumor. However, the characteristic genetic alterations between the primary gastric cancer and its metastatic ovarian tumor have not been studied. We used laser capture microdissection to procure tissues from 7 patients with gastric cancer who had ovarian metastases (Krukenberg tumor) and tissues from 14 patients with gastric cancer without ovarian metastases. Loss of heterozygosity (LOH) analysis was performed by use of 16 polymorphic markers, which are mapped to the FHIT, APC, p16, BRCA2, E-cadherin, p53, BRCA1, and DPC4 loci. Immunohistochemical staining with anti-Fhit antibody was performed in 7 Krukenberg tumors and 92 gastric cancers without ovarian metastases. LOH at the FHIT locus was observed in six (85.7%) of the seven Krukenberg tumors. In contrast, the gastric cancers without ovarian metastases showed a lower frequency (28.6%, 4/14) of LOH at the FHIT locus (p Ͻ 0.05, odds ratio ϭ 1/15). Anti-Fhit antibody showed that expression of Fhit was lost in each of the 7 (100%) Krukenberg tumors but in only 41 (44.6%) of the 92 patients who had gastric cancer without ovarian metastases (p Ͻ 0.05; odds ratio ϭ 1/18.614). Further analysis showed that loss of Fhit expression is highly associated with signet-ring cell type gastric cancer (p Ͻ 0.0001, odds ratio ϭ 62.5) but is not correlated with prognosis. Alteration of the FHIT gene is a characteristic of signet-ring cell type gastric cancer and Krukenberg tumor. (Lab Invest 2002, 82:1201–1208). astric cancer is a leading cause of cancer death plasia to cancer. The signet-ring cell subtype of gas- G in the world despite a trend toward decreasing tric cancer is so named because of the shape of the incidence in most countries (Fuchs and Mayer, 1995). tumor cells and is characterized by infiltration of Markedly clinical and biologic heterogeneity has been individual cells. noted among different subtypes of gastric cancer. Gastric cancer of youth is predominantly a disease Gastric cancer consists of intestinal and diffuse sub- of women, especially among Asians (Tamura and types according to Lauren’s classification (Lauren, Curtiss, 1960). It is usually of the signet-ring cell rather 1965) and can be categorized as signet-ring cell and than the gland-forming subtype and has a predilection non–signet-ring cell cancer according to the World for metastasizing to the ovaries (Duarte and Llanos, Health Organization (WHO) histologic classification 1981; Holtz and Hart, 1982). When gastric cancer (Oota and Sobin, 1990). Different subtypes of gastric metastasizes to the ovary, the tumor is named a cancer differ not only in morphology but also in their Krukenberg tumor, which is characterized by pleomor- clinical and epidemiologic characteristics. phic mucin-filled signet-ring cells accompanied by a The intestinal subtype of gastric cancer predomi- sarcomatoid proliferation of the ovarian stroma (Serov nates in high-risk populations, is more frequently et al, 1973). Krukenberg tumors commonly arise in found in elderly patients, and is characterized by a premenopausal women and have a poor prognosis histologic pattern that mimics large-bowel adenocar- (Gilliland and Gill, 1992; McGill et al, 1999). However, cinoma. The diffuse type of gastric cancer is less the mechanism by which this particular subtype of common, occurring in relatively low-risk populations gastric cancer metastasizes to the ovaries remains and mostly in younger individuals or those of blood unknown. Recent molecular and epidemiologic stud- type A (Wu et al, 1997). Different precancerous lesions ies suggest that different subtypes of gastric cancer probably exist for these two types. The intestinal type have different genetic changes (Tahara, 1993; Wright of gastric cancer follows the proposed sequential et al, 1992; Wu et al, 2001). However, the character- changes from gastritis, intestinal metaplasia, and dys- istic genetic alterations between the primary gastric cancer and its metastatic ovarian tumor have not been studied. DOI: 10.1097/01.LAB.0000028060.37763.D5 In this study, we explored the genetic alterations of Received April 22, 2002. gastric cancer and its metastatic ovarian tumor by Address reprint requests to: Dr. Jaw-Town Lin, Department of Internal analyzing loss of heterozygosity (LOH) with different Medicine, National Taiwan University Hospital, No. 7, Chung-Shan microsatellite markers. To avoid stromal cell contam- South Road, Taipei, Taiwan. E-mail: [email protected] ination, we used laser capture microdissection (LCM) Laboratory Investigation • September 2002 • Volume 82 • Number 9 1201 Chang et al to procure primary gastric tumor cells and metastatic allele in gastric cancer and metastatic ovarian tumor ovarian tumor cells that were as pure as possible for cells (Fig. 1). Cases 2, 3, and 7 had LOH only in the genetic analysis. Immunohistochemical staining (IHS) metastatic ovarian tumors and not in the primary of Fhit (fragile histidine triad) protein was preformed in gastric cancers. gastric cancers with and without ovarian metastases. We found that LOH at the FHIT locus was observed in Immunochemical Staining for Fhit Expression in Different the great majority of Krukenberg tumors but infre- Subtypes of Gastric Cancer quently in gastric cancers without ovarian metastases. As expected, loss of Fhit expression was detected in To explore the role of FHIT further, we performed IHS the majority of Krukenberg tumors and in only one half with anti-Fhit antibody in the 7 Krukenberg tumors and of gastric cancers without ovarian metastases. Alter- the 92 gastric cancers without ovarian metastases ation of the FHIT gene is a characteristic of Kruken- (Fig. 2). All of the Krukenberg tumors exhibited loss of berg tumors and of the signet-ring cell type of gastric Fhit expression in both gastric and ovarian tumors cancer. (Tables 3 and 4). Only 41 (44.6%) of the 92 patients who had gastric cancer without ovarian metastases Results exhibited loss of Fhit expression (p ϭ 0.005; odds ratio ϭ 1/18.614) (Table 4). Loss of Fhit expression was The demographic characteristics of the 99 patients are more frequently found in diffuse-type and in mixed- summarized in Table 1. The predominance of female type cancers (65.0% and 60%, respectively) than in patients and those of young age was noted for Kruke- the intestinal-type cancers (22.7%) (p Ͻ 0.05). There nberg tumors. The ages of patients with Krukenberg was a significant difference in Fhit expression between tumors ranged from 42 to 55 years, with a mean of intestinal-type cancers and Krukenberg tumors (p ϭ 45.9 years. In addition, a younger age was observed in 0.002; odds ratio ϭ 1/49.286, with 95% confidence the signet-ring cell group, with a mean of 52.4 years, interval 0.001–0.386). However, no statistically signif- when compared with the non–signet-ring cell group, icant difference was observed between Krukenberg with a mean of 59.5 years (p Ͻ 0.05). Nevertheless, tumors and diffuse-type or mixed-type cancers (Table although there is a suggestion of female preponder- 4). ance, the gender difference is not significant between To clarify whether alteration of Fhit expression is signet-ring cell and non–signet-ring cell groups (p ϭ specific for the existence of ovarian metastases of 0.25) (Table 1). gastric cancer or a specific histologic subtype, we divided the 99 patients (7 Krukenberg tumors and 92 gastric cancers without ovarian metastases) into two Heterogeneity and Preferential LOH at the FHIT Locus in Krukenberg Tumor groups according to the WHO classification. Eighteen cancers were classified as signet-ring cell subtype, LOH affecting the FHIT gene could be observed in six and the remaining 81 belonged to the non–signet-ring (85.7%) of the seven Krukenberg tumors. In contrast, cell subtype. All seven Krukenberg tumors belonged gastric cancers without ovarian metastases demon- to the signet-ring cell subtype. Eighteen (100%) pa- strated a lower frequency (28.6%, 4/14) of LOH at the tients with signet-ring cell type cancer showed loss of FHIT locus (p ϭ 0.024) (Table 2). Four cases of Fhit expression, whereas 30 (37%) patients with non– Krukenberg tumor (Cases 1, 2, 3, and 7) revealed a signet-ring cell type cancer showed loss of Fhit ex- discrepancy between primary gastric cancers and pression (p Ͻ 0.0001; odds ratio 62.5, 95% confi- metastatic ovarian tumors in the LOH pattern at the dence interval 3.636–1000) (Table 4). The Fhit FHIT locus (Table 3). Case 1 had LOH at a different expression between signet-ring cell type gastric can- Table 1. Demographic Characteristics of 99 Patients with Gastric Cancer, Stratified by Histologic Subtype Age Sex Gastric cancer n Mean (range) Men:women WHO histologic classification 99 58.2 (26–86) 56:43 Non–signet-ring cell type 81 59.5 (26–86)a 48:33c Signet-ring cell type 18 52.4 (33–80) 8:10 Krukenberg tumor 7 45.9 (42–55) 0:7 Gastric cancer without ovarian metastasis 11 56.5 (33–80)b 8:3 Lauren’s classification 92 59.2 (26–86) 56:36 Intestinal type 44 63.0 (26–86) 30:14 Diffuse type 43 56.0 (33–84) 23:20 Mixed type 5 52.4 (36–68) 3:2 WHO, World Health Organization.
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