Cancer Res Treat.  2005 Feb;37(1):1-19.

Biology of SNU Cell Lines

• Ku JL
• Park JG

Abstract

SNU (Seoul National University) cell lines have been established from Korean cancer patients since 1982. Of these 109 cell lines have been characterized and reported, i.e., 17 colorectal carcinoma, 12 hepatocellular carcinoma, 11 gastric carcinoma, 12 uterine cervical carcinoma, 17 B-lymphoblastoid cell lines derived from cancer patients, 5 ovarian carcinoma, 3 malignant mixed Mllerian tumor, 6 laryngeal squamous cell carcinoma, 7 renal cell carcinoma, 9 brain tumor, 6 biliary tract, and 4 pancreatic carcinoma cell lines. These SNU cell lines have been distributed to biomedical researchers domestic and worldwide through the KCLB (Korean Cell Line Bank), and have proven to be of value in various scientific research fields. The characteristics of these cell lines have been reported in over 180 international journals by our laboratory and by many other researchers from 1987. In this paper, the cellular and molecular characteristics of SNU human cancer cell lines are summarized according to their genetic and epigenetic alterations and functional analysis.

Keyword

SNU; Cell line; Cell culture; Cancer; Cancer research

MeSH Terms

Biliary Tract
Biology*
Brain Neoplasms
Carcinoma, Hepatocellular
Carcinoma, Renal Cell
Carcinoma, Squamous Cell
Cell Culture Techniques
Cell Line*
Colorectal Neoplasms
Epigenomics
Humans

Figure

• 

  Fig. 1 Procedure for the establishment of cancer cell lines.

• 

  Fig. 2 Culture of SNU cell lines. (A) SNU-16 gastric cancer cell line (B) SNU-17 uterine cervical carcinoma cell line (C) SNU-251 ovarian carcinoma cell line (D) SNU-245 biliary tract cancer cell line (E) SNU-368 hepatocellular carcinoma cell line (F) SNU-482 renal cell carcinoma cell line (G) SNU-668 gastric carcinoma cell line (H) SNU-1033 colorectal carcinoma cell line (I) SNU-175 colorectal carcinoma cell line (J) SNU-1 gastric cancer cell line cultured in soft agar.

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111. Jang JH, Shin KH, Park JG. Mutations in fibroblast growth factor receptor 2 and fibroblast growth factor receptor 3 genes associated with human gastric and colorectal cancers. Cancer Res. 2001; 61:3541–3543. PMID: 11325814.

112. Shin EY, Ma EK, Kim CK, Kwak SJ, Kim EG. Src/ERK but not phospholipase D is involved in keratinocyte growth factor-stimulated secretion of matrix metalloprotease-9 and urokinase-type plasminogen activator in SNU-16 human stomach cancer cell. J Cancer Res Clin Oncol. 2002; 128:596–602. PMID: 12458339.

113. Hwang IR, Hsu PI, Peterson LE, Gutierrez O, Kim JG, Graham DY, et al. Interleukin-6 genetic polymorphisms are not related to Helicobacter pylori-associated gastroduodenal diseases. Helicobacter. 2003; 8:142–148. PMID: 12662382.

114. Jung HC, Kim JM, Song IS, Kim CY. Helicobacter pylori induces an array of pro-inflammatory cytokines in human gastric epithelial cells: quantification of mRNA for interleukin-8, -1 alpha/beta, granulocyte-macrophage colony-stimulating factor, monocyte chemoattractant protein-1 and tumour necrosis factor-alpha. J Gastroenterol Hepatol. 1997; 12:473–480. PMID: 9257236.

115. Kim JM, Kim JS, Jung HC, Oh YK, Kim N, Song IS. Inhibition of Helicobacter pylori-induced nuclear factor-kappa B activation and interleukin-8 gene expression by ecabet sodium in gastric epithelial cells. Helicobacter. 2003; 8:542–553. PMID: 14536001.

116. Kim JM, Kim JS, Jung HC, Song IS, Kim CY. Upregulated cyclooxygenase-2 inhibits apoptosis of human gastric epithelial cells infected with Helicobacter pylori. Dig Dis Sci. 2000; 45:2436–2443. PMID: 11258572.

117. Kim JM, Kim JS, Jung HC, Song IS, Kim CY. Up-regulation of inducible nitric oxide synthase and nitric oxide in Helicobacter pylori-infected human gastric epithelial cells: possible role of interferon-gamma in polarized nitric oxide secretion. Helicobacter. 2002; 7:116–128. PMID: 11966872.

118. Shin KH, Han HJ, Park JG. Growth suppression mediated by transfection of wild-type hMLH1 in human cancer cells expressing endogenous truncated hMLH1 protein. Int J Oncol. 1998; 12:609–615. PMID: 9472100.

119. Shin KH, Yang YM, Park JG. Absence or decreased levels of the hMLH1 protein in human gastric carcinoma cell lines: implication of hMLH1 in alkylation tolerance. J Cancer Res Clin Oncol. 1998; 124:421–426. PMID: 9750018.

120. Park IC, Park MJ, Rhee CH, Lee JI, Choe TB, Jang JJ, et al. Protein kinase C activation by PMA rapidly induces apoptosis through caspase-3/CPP32 and serine protease(s) in a gastric cancer cell line. Int J Oncol. 2001; 18:1077–1083. PMID: 11295059.

121. Yang Z, Liu S, Chen X, Chen H, Huang M, Zheng J. Induction of apoptotic cell death and in vivo growth inhibition of human cancer cells by a saturated branched-chain fatty acid, 13-methyltetradecanoic acid. Cancer Res. 2000; 60:505–509. PMID: 10676625.

122. Nam SY, Jung GA, Hur GC, Chung HY, Kim WH, Seol DW, et al. Upregulation of FLIP(S) by Akt, a possible inhibition mechanism of TRAIL-induced apoptosis in human gastric cancers. Cancer Sci. 2003; 94:1066–1073. PMID: 14662022.

123. Lee TB, Min YD, Lim SC, Kim KJ, Jeon HJ, Choi SM, et al. Fas (Apo-1/CD95) and Fas ligand interaction between gastric cancer cells and immune cells. J Gastroenterol Hepatol. 2002; 17:32–38. PMID: 11895550.

124. Jeong JH, Park JS, Moon B, Kim MC, Kim JK, Lee S, et al. Orphan nuclear receptor Nur77 translocates to mitochondria in the early phase of apoptosis induced by synthetic chenodeoxycholic acid derivatives in human stomach cancer cell line SNU-1. Ann N Y Acad Sci. 2003; 1010:171–177. PMID: 15033715.

125. Park IK, Kim BJ, Goh YJ, Lyu MA, Park CG, Hwang ES, et al. Co-expression of urokinase-type plasminogen activator and its receptor in human gastric-cancer cell lines correlates with their invasiveness and tumorigenicity. Int J Cancer. 1997; 71:867–873. PMID: 9180158.

126. Rabenau KE, O'Toole JM, Bassi R, Kotanides H, Witte L, Ludwig DL, et al. DEGA/AMIGO-2, a leucine-rich repeat family member, differentially expressed in human gastric adenocarcinoma: effects on ploidy, chromosomal stability, cell adhesion/migration and tumorigenicity. Oncogene. 2004; 23:5056–5067. PMID: 15107827.

127. Shin BA, Yoo HG, Kim HS, Kim MH, Hwang YS, Chay KO, et al. P38 MAPK pathway is involved in the urokinase plasminogen activator expression in human gastric SNU-638 cells. Oncol Rep. 2003; 10:1467–1471. PMID: 12883725.

128. Lee DH, Yang Y, Lee SJ, Kim KY, Koo TH, Shin SM, et al. Macrophage inhibitory cytokine-1 induces the invasiveness of gastric cancer cells by up-regulating the urokinase-type plasminogen activator system. Cancer Res. 2003; 63:4648–4655. PMID: 12907645.

129. Cho YG, Nam SW, Kim TY, Kim YS, Kim CJ, Park JY, et al. Overexpression of S100A4 is closely related to the aggressiveness of gastric cancer. Apmis. 2003; 111:539–545. PMID: 12887505.

130. Zhang H, Wu J, Meng L, Shou CC. Expression of vascular endothelial growth factor and its receptors KDR and Flt-1 in gastric cancer cells. World J Gastroenterol. 2002; 8:994–998. PMID: 12439912.

131. Kim IJ, Park JH, Kang HC, Shin Y, Park HW, Park HR, et al. Mutational analysis of BRAF and K-ras in gastric cancers: absence of BRAF mutations in gastric cancers. Hum Genet. 2003; 114:118–120. PMID: 14513361.

132. Kim JH, Takahashi T, Chiba I, Park JG, Birrer MJ, Roh JK, et al. Occurrence of p53 gene abnormalities in gastric carcinoma tumors and cell lines. J Natl Cancer Inst. 1991; 83:938–943. PMID: 1676761.

133. Shin KH, Park JG. Microsatellite instability is associated with genetic alteration but not with low levels of expression of the human mismatch repair proteins hMSH2 and hMLH1. Eur J Cancer. 2000; 36:925–931. PMID: 10785599.

134. Lee YY, Kang SH, Seo JY, Jung CW, Lee KU, Choe KJ, et al. Alterations of p16INK4A and p15INK4B genes in gastric carcinomas. Cancer. 1997; 80:1889–1896. PMID: 9366289.

135. Guilford PJ, Hopkins JB, Grady WM, Markowitz SD, Willis J, Lynch H, et al. E-cadherin germline mutations define an inherited cancer syndrome dominated by diffuse gastric cancer. Hum Mutat. 1999; 14:249–255. PMID: 10477433.

136. Sakakura C, Hagiwara A, Nakanishi M, Shimomura K, Takagi T, Yasuoka R, et al. Differential gene expression profiles of gastric cancer cells established from primary tumour and malignant ascites. Br J Cancer. 2002; 87:1153–1161. PMID: 12402156.

137. Sakakura C, Simomura K, Shuichi K, Nakase Y, Fukuda K, Takagi T, et al. [Screening of novel biomarkers for the detection of intraperitoneally disseminated cancer cells using human cDNA microarray]. Gan To Kagaku Ryoho. 2002; 29:2271–2274. PMID: 12484052.

138. Lee HS, Park MH, Yang SJ, Jung HY, Byun SS, Lee DS, et al. Gene expression analysis in human gastric cancer cell line treated with trichostatin A and S-Adenosyl-L-homocysteine using cDNA microarray. Biol Pharm Bull. 2004; 27:1497–1503. PMID: 15467184.

139. Shin JH, Chung J, Kim HO, Kim YH, Hur YM, Rhim JH, et al. Detection of cancer cells in peripheral blood of stomach cancer patients using RT-PCR amplification of tumour-specific mRNAs. Aliment Pharmacol Ther. 2002; 16(Suppl 2):137–144. PMID: 11966534.

140. Shin JY, Kim HS, Park J, Park JB, Lee JY. Mechanism for inactivation of the KIP family cyclin-dependent kinase inhibitor genes in gastric cancer cells. Cancer Res. 2000; 60:262–265. PMID: 10667572.

141. Jeong YW, Kim KS, Oh JY, Park JC, Baek WK, Suh SI, et al. Exogenous wild-type p16INK4A gene induces delayed cell proliferation and promotes chemosensitivity through decreased pRB and increased E2F-1 expressions. Int J Mol Med. 2003; 12:61–65. PMID: 12792810.

142. Choi CH. Cloning and functional study of a novel human metallothionein-I isoform induced by paraquat. Biochem Biophys Res Commun. 2003; 304:236–240. PMID: 12711304.

143. Han SH, Jeon JH, Ju HR, Jung U, Kim KY, Yoo HS, et al. VDUP1 upregulated by TGF-beta1 and 1,25-dihydorxyvitamin D3 inhibits tumor cell growth by blocking cell-cycle progression. Oncogene. 2003; 22:4035–4046. PMID: 12821938.

144. Park BK, Moon HR, Yu JR, Kook J, Chai JY, Lee SH. [Comparative susceptibility of different cell lines for culture of Toxoplasma gondii in vitro]. Korean J Parasitol. 1993; 31:215–222. PMID: 8241080.

145. Leung WK, Kim JJ, Wu L, Sepulveda JL, Sepulveda AR. Identification of a second MutL DNA mismatch repair complex (hPMS1 and hMLH1) in human epithelial cells. J Biol Chem. 2000; 275:15728–15732. PMID: 10748105.

146. Yamamoto H, Itoh F, Fukushima H, Hinoda Y, Imai K. Overexpression of cyclooxygenase-2 protein is less frequent in gastric cancers with microsatellite instability. Int J Cancer. 1999; 84:400–403. PMID: 10404093.

147. Bae SI, Park JG, Kim YI, Kim WH. Genetic alterations in gastric cancer cell lines and their original tissues. Int J Cancer. 2000; 87:512–516. PMID: 10918190.

148. Woo DK, Kim HS, Lee HS, Kang YH, Yang HK, Kim WH. Altered expression and mutation of beta-catenin gene in gastric carcinomas and cell lines. Int J Cancer. 2001; 95:108–113. PMID: 11241321.

149. Oh ST, Seo JS, Moon UY, Kang KH, Shin DJ, Yoon SK, et al. A naturally derived gastric cancer cell line shows latency I Epstein-Barr virus infection closely resembling EBV-associated gastric cancer. Virology. 2004; 320:330–336. PMID: 15016554.

150. Han SU, Kim HT, Seong do H, Kim YS, Park YS, Bang YJ, et al. Loss of the Smad3 expression increases susceptibility to tumorigenicity in human gastric cancer. Oncogene. 2004; 23:1333–1341. PMID: 14647420.

151. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, et al. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell. 2002; 109:113–124. PMID: 11955451.

152. Kang MS, Lee HJ, Lee JH, Ku JL, Lee KP, Kelley MJ, et al. Mutation of p53 gene in hepatocellular carcinoma cell lines with HBX DNA. Int J Cancer. 1996; 67:898–902. PMID: 8824565.

153. Kim SO, Park JG, Lee YI. Increased expression of the insulin-like growth factor I (IGF-I) receptor gene in hepatocellular carcinoma cell lines: implications of IGF-I receptor gene activation by hepatitis B virus X gene product. Cancer Res. 1996; 56:3831–3836. PMID: 8706031.

154. Cho JW, Jeong YW, Han SW, Park JB, Jang BC, Baek WK, et al. Aberrant p16INK4A RNA transcripts expressed in hepatocellular carcinoma cell lines regulate pRb phosphorylation by binding with CDK4, resulting in delayed cell cycle progression. Liver Int. 2003; 23:194–200. PMID: 12955883.

155. Suh SI, Pyun HY, Cho JW, Baek WK, Park JB, Kwon T, et al. 5-Aza-2'-deoxycytidine leads to down-regulation of aberrant p16INK4A RNA transcripts and restores the functional retinoblastoma protein pathway in hepatocellular carcinoma cell lines. Cancer Lett. 2000; 160:81–88. PMID: 11098088.

156. Huang JZ, Xia SS, Ye QF, Jiang HY, Chen ZH. Effects of p16 gene on biological behaviours in hepatocellular carcinoma cells. World J Gastroenterol. 2003; 9:84–88. PMID: 12508357.

157. Chun E, Lee KY. Bcl-2 and Bcl-xL are important for the induction of paclitaxel resistance in human hepatocellular carcinoma cells. Biochem Biophys Res Commun. 2004; 315:771–779. PMID: 14975768.

158. Hwang HJ, Kim GJ, Lee GB, Oh JT, Chun YH, Park SH. A comprehensive karyotypic analysis on Korean hepatocellular carcinoma cell lines by cross-species color banding and comparative genomic hybridization. Cancer Genet Cytogenet. 2003; 141:128–137. PMID: 12606130.

159. Scharf JG, Dombrowski F, Ramadori G. The IGF axis and hepatocarcinogenesis. Mol Pathol. 2001; 54:138–144. PMID: 11376124.

160. Shin EC, Ahn JM, Kim CH, Choi Y, Ahn YS, Kim H, et al. IFN-gamma induces cell death in human hepatoma cells through a TRAIL/death receptor-mediated apoptotic pathway. Int J Cancer. 2001; 93:262–268. PMID: 11410875.

161. Shin EC, Shin JS, Park JH, Kim H, Kim SJ. Expression of fas ligand in human hepatoma cell lines: role of hepatitis-B virus X (HBX) in induction of Fas ligand. Int J Cancer. 1999; 82:587–591. PMID: 10404075.

162. Shin EC, Shin WC, Choi Y, Kim H, Park JH, Kim SJ. Effect of interferon-gamma on the susceptibility to Fas (CD95/APO-1)-mediated cell death in human hepatoma cells. Cancer Immunol Immunother. 2001; 50:23–30. PMID: 11315506.

163. Park SS, Eom YW, Kim EH, Lee JH, Min do S, Kim S, et al. Involvement of c-Src kinase in the regulation of TGF-beta1-induced apoptosis. Oncogene. 2004; 23:6272–6281. PMID: 15208664.

164. Baek WK, Kim D, Jung N, Yi YW, Kim JM, Cha SD, et al. Increased expression of cyclin G1 in leiomyoma compared with normal myometrium. Am J Obstet Gynecol. 2003; 188:634–639. PMID: 12634633.

165. Foli A, Benvenuto F, Piccinini G, Bareggi A, Cossarizza A, Lisziewicz J, et al. Direct analysis of mitochondrial toxicity of antiretroviral drugs. Aids. 2001; 15:1687–1694. PMID: 11546944.

166. Lee H, Lee SI, Cho J, Choi SU, Yang SI. Synthesis and in vitro evaluation of 1,8-diazaanthraquinones bearing 3-dialkylaminomethyl or 3-(N-alkyl- or N-aryl)carbamoyloxymethyl substituent. Eur J Med Chem. 2003; 38:695–702. PMID: 12932900.

167. Lee SW, Lee YM, Bae SK, Murakami S, Yun Y, Kim KW. Human hepatitis B virus X protein is a possible mediator of hypoxia-induced angiogenesis in hepatocarcinogenesis. Biochem Biophys Res Commun. 2000; 268:456–461. PMID: 10679226.

168. Ferber MJ, Montoya DP, Yu C, Aderca I, McGee A, Thorland EC, et al. Integrations of the hepatitis B virus (HBV) and human papillomavirus (HPV) into the human telomerase reverse transcriptase (hTERT) gene in liver and cervical cancers. Oncogene. 2003; 22:3813–3820. PMID: 12802289.

169. Moon MS, Lee CJ, Um SJ, Park JS, Yang JM, Hwang ES. Effect of BPV1 E2-mediated inhibition of E6/E7 expression in HPV16-positive cervical carcinoma cells. Gynecol Oncol. 2001; 80:168–175. PMID: 11161855.

170. Baykal A, Rosen D, Zhou C, Liu J, Sahin AA. Telomerase in breast cancer: a critical evaluation. Adv Anat Pathol. 2004; 11:262–268. PMID: 15322492.

171. Zhou C, Smith JL, Liu J. Role of BRCA1 in cellular resistance to paclitaxel and ionizing radiation in an ovarian cancer cell line carrying a defective BRCA1. Oncogene. 2003; 22:2396–2404. PMID: 12717416.

172. Campbell M, Qu S, Wells S, Sugandha H, Jensen RA. An adenoviral vector containing an arg-gly-asp (RGD) motif in the fiber knob enhances protein product levels from transgenes refractory to expression. Cancer Gene Ther. 2003; 10:559–570. PMID: 12833136.

173. Park SH, Park SY, Kim DW, Chun YH. Chromosomal aberrations in ovarian malignant brenner tumor cell line using chromosome painting. Cancer Genet Cytogenet. 2000; 118:151–153. PMID: 10748297.

174. Yu S, Lee M, Shin S, Park J. Apoptosis induced by progesterone in human ovarian cancer cell line SNU-840. J Cell Biochem. 2001; 82:445–451. PMID: 11500921.

175. Chang SH, Kim SH, Lee WK, Kim HJ, Choi SH, Park JH, et al. Cloning and analysis of the Epstein-Barr virus glycoprotein 350 genes. Mol Cells. 1998; 8:585–593. PMID: 9856346.

176. Kim HR, Jeong JA, Park CH, Lee SK, Lee WK, Jang YS. A role for cell cycle proteins in the serum-starvation resistance of Epstein-Barr virus immortalized B lymphocytes. Biochem Cell Biol. 2002; 80:407–413. PMID: 12234093.

177. Lee W, Hwang YH, Lee SK, Subramanian C, Robertson ES. An Epstein-Barr virus isolated from a lymphoblastoid cell line has a 16-kilobase-pair deletion which includes gp350 and the Epstein-Barr virus nuclear antigen 3A. J Virol. 2001; 75:8556–8568. PMID: 11507201.

178. Park CH, Kim HR, Kim J, Jang SH, Lee KY, Chung GH, et al. Latent membrane protein 1 of Epstein-Barr virus plays an important role in the serum starvation resistance of Epstein-Barr virus-immortalized B lymphocytes. J Cell Biochem. 2004; 91:777–785. PMID: 14991769.

179. Koh TY, Park SW, Park KH, Lee SG, Seol JG, Lee DW, et al. Inhibitory effect of p27KIP1 gene transfer on head and neck squamous cell carcinoma cell lines. Head Neck. 2003; 25:44–49. PMID: 12478543.

180. Park SW, Lee SG, Song SH, Heo DS, Park BJ, et al. The effect of nitric oxide on cyclooxygenase-2 (COX-2) overexpression in head and neck cancer cell lines. Int J Cancer. 2003; 107:729–738. PMID: 14566822.

181. Rhee CS, Sen M, Lu D, Wu C, Leoni L, Rubin J, et al. Wnt and frizzled receptors as potential targets for immunotherapy in head and neck squamous cell carcinomas. Oncogene. 2002; 21:6598–6605. PMID: 12242657.

182. Chung PS, Kim HG, Rhee CK, Saxton RE. Anticancer effect of combined intratumor cisplatin injection and interstitial KTP laser therapy on xenografted squamous cell carcinoma. J Clin Laser Med Surg. 2003; 21:23–27. PMID: 12614556.

183. Sung MW, Roh JL, Park BJ, Park SW, Kwon TK, Lee SJ, et al. Bile acid induces cyclo-oxygenase-2 expression in cultured human pharyngeal cells: a possible mechanism of carcinogenesis in the upper aerodigestive tract by laryngopharyngeal reflux. Laryngoscope. 2003; 113:1059–1063. PMID: 12782823.

184. Kang YH, Lee E, Choi MK, Ku JL, Kim SH, Park YG, et al. Role of reactive oxygen species in the induction of apoptosis by alpha-tocopheryl succinate. Int J Cancer. 2004; 112:385. PMID: 15382062.

185. Hansel DE, Rahman A, Hidalgo M, Thuluvath PJ, Lillemoe KD, Shulick R, et al. Identification of novel cellular targets in biliary tract cancers using global gene expression technology. Am J Pathol. 2003; 163:217–229. PMID: 12819026.