Overexpression of S100A4 in human cancer cell lines resistant to methotrexate

BMC Cancer

Volumn 10, Issue , 2010, Pages

  Mencía, Nuria ^a   Selga, Elisabet ^a   Rico, Isabel ^a   de Almagro, M Cristina ^a   Villalobos, Xenia ^a   Ramirez, Sara ^a   Adan, Jaume ^b   Hernández, Jose L ^b   Noé, Véronique ^a   Ciudad, Carlos J ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b LEITAT TECHNOLOGICAL CENTER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALVASCULIN; MESSENGER RNA; METHOTREXATE; SMALL INTERFERING RNA; WNT PROTEIN; ANTINEOPLASTIC ANTIMETABOLITE; PROTEIN S 100; S100A4 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL LEVEL; COLON CANCER; CONTROLLED STUDY; DNA MICROARRAY; DRUG MECHANISM; EXPRESSION VECTOR; EXTRACELLULAR SPACE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; WESTERN BLOTTING; CELL STRAIN CACO 2; CELL STRAIN HT29; CELL SURVIVAL; COLON TUMOR; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METHODOLOGY; PATHOLOGY; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANTIMETABOLITES, ANTINEOPLASTIC; BETA CATENIN; BLOTTING, WESTERN; CACO-2 CELLS; CELL SURVIVAL; COLONIC NEOPLASMS; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; METHOTREXATE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; S100 PROTEINS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

EID: 77954654381     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-10-250     Document Type: Article

References (54)

1. Chu E, Grem JL, Johnston PG, Allegra CJ. New concepts for the development and use of antifolates. Stem Cells 1996, 14:41-46. 10.1002/stem.140041, 8820950.
2. Jolivet J, Cowan KH, Curt GA, Clendeninn NJ, Chabner BA. The pharmacology and clinical use of methotrexate. N Engl J Med 1983, 309:1094-1104.
3. Selga E, Oleaga C, Ramirez S, de Almagro MC, Noe V, Ciudad CJ. Networking of differentially expressed genes in human cancer cells resistant to methotrexate. Genome Med 2009, 1:83. 10.1186/gm83, 2768990, 19732436.
4. Selga E, Noe V, Ciudad CJ. Transcriptional regulation of aldo-keto reductase 1C1 in HT29 human colon cancer cells resistant to methotrexate: role in the cell cycle and apoptosis. Biochem Pharmacol 2008, 75:414-426. 10.1016/j.bcp.2007.08.034, 17945194.
5. Selga E, Morales C, Noe V, Peinado MA, Ciudad CJ. Role of caveolin 1, E-cadherin, Enolase 2 and PKCalpha on resistance to methotrexate in human HT29 colon cancer cells. BMC Med Genomics 2008, 1:35. 10.1186/1755-8794-1-35, 2527490, 18694510.
6. Moore BW. A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 1965, 19:739-744. 10.1016/0006-291X(65)90320-7, 4953930.
7. Dukhanina EA, Dukhanin AS, Lomonosov MY, Lukanidin EM, Georgiev GP. Spectral studies on the calcium-binding properties of Mts1 protein and its interaction with target protein. FEBS Lett 1997, 410:403-406. 10.1016/S0014-5793(97)00576-0, 9237671.
8. Donato R. Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 2003, 60:540-551. 10.1002/jemt.10296, 12645002.
9. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001, 33:637-668. 10.1016/S1357-2725(01)00046-2, 11390274.
10. Parker C, Whittaker PA, Usmani BA, Lakshmi MS, Sherbet GV. Induction of 18A2/mts1 gene expression and its effects on metastasis and cell cycle control. DNA Cell Biol 1994, 13:1021-1028. 10.1089/dna.1994.13.1021, 7945934.
11. Lloyd BH, Platt-Higgins A, Rudland PS, Barraclough R. Human S100A4 (p9Ka) induces the metastatic phenotype upon benign tumour cells. Oncogene 1998, 17:465-473. 10.1038/sj.onc.1201948, 9696040.
12. Ambartsumian N, Klingelhofer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E, Georgiev G, Berezin V, Bock E, Rygaard J, et al. The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 2001, 20:4685-4695. 10.1038/sj.onc.1204636, 11498791.
13. Mahon PC, Baril P, Bhakta V, Chelala C, Caulee K, Harada T, Lemoine NR. S100A4 contributes to the suppression of BNIP3 expression, chemoresistance, and inhibition of apoptosis in pancreatic cancer. Cancer Res 2007, 67:6786-6795. 10.1158/0008-5472.CAN-07-0440, 17638890.
14. Rocke DM, Durbin B. A model for measurement error for gene expression arrays. J Comput Biol 2001, 8:557-569. 10.1089/106652701753307485, 11747612.
15. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63. 10.1016/0022-1759(83)90303-4, 6606682.
16. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
17. Schmidt-Hansen B, Klingelhofer J, Grum-Schwensen B, Christensen A, Andresen S, Kruse C, Hansen T, Ambartsumian N, Lukanidin E, Grigorian M. Functional significance of metastasis-inducing S100A4(Mts1) in tumor-stroma interplay. J Biol Chem 2004, 279:24498-24504. 10.1074/jbc.M400441200, 15047714.
18. Stein U, Arlt F, Walther W, Smith J, Waldman T, Harris ED, Mertins SD, Heizmann CW, Allard D, Birchmeier W, et al. The metastasis-associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 2006, 131:1486-1500. 10.1053/j.gastro.2006.08.041, 17101323.
19. Sherbet GV, Lakshmi MS. S100A4 (MTS1) calcium binding protein in cancer growth, invasion and metastasis. Anticancer Res 1998, 18:2415-2421.
20. Sherbet G. Metastasis promoter S100A4 is a potentially valuable molecular target for cancer therapy. Cancer Letters 2009, 280:15-30. 10.1016/j.canlet.2008.10.037, 19059703.
21. Takenaga K, Nakanishi H, Wada K, Suzuki M, Matsuzaki O, Matsuura A, Endo H. Increased expression of S100A4, a metastasis-associated gene, in human colorectal adenocarcinomas. Clin Cancer Res 1997, 3:2309-2316.
22. Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L, Barraclough R. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 2000, 60:1595-1603.
23. Pedersen KB, Nesland JM, Fodstad O, Maelandsmo GM. Expression of S100A4, E-cadherin, alpha- and beta-catenin in breast cancer biopsies. Br J Cancer 2002, 87:1281-1286. 10.1038/sj.bjc.6600624, 2408909, 12439718.
24. Schuyer M, Henzen-Logmans SC, van der Burg ME, Fieret JH, Derksen C, Look MP, Meijer-van Gelder ME, Klijn JG, Foekens JA, Berns EM. Genetic alterations in ovarian borderline tumours and ovarian carcinomas. Eur J Obstet Gynecol Reprod Biol 1999, 82:147-150. 10.1016/S0301-2115(98)00217-6, 10206406.
25. Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, Kobayashi K, Matsuzuka F, Kakudo K, Kuma K, Miyauchi A. S100A4 expression is an early event of papillary carcinoma of the thyroid. Oncology 2004, 67:397-402. 10.1159/000082924, 15713996.
26. Rosty C, Ueki T, Argani P, Jansen M, Yeo CJ, Cameron JL, Hruban RH, Goggins M. Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol 2002, 160:45-50. 1867115, 11786397.
27. Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, Sasaki T. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int J Oncol 2000, 16:1125-1131.
28. Takenaga K, Nakamura Y, Sakiyama S. Expression of antisense RNA to S100A4 gene encoding an S100-related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene 1997, 14:331-337. 10.1038/sj.onc.1200820, 9018119.
29. Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, Fujimura T, Nishimura G, Tani T, Shimizu K, et al. Increased expression of S100A4 and its prognostic significance in esophageal squamous cell carcinoma. Int J Oncol 2001, 18:715-720.
30. Gupta S, Hussain T, MacLennan GT, Fu P, Patel J, Mukhtar H. Differential expression of S100A2 and S100A4 during progression of human prostate adenocarcinoma. J Clin Oncol 2003, 21:106-112. 10.1200/JCO.2003.03.024, 12506178.
31. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K, Kinoshita K, Ninomiya I, Sugiyama K, Heizmann CW, et al. Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 2000, 6:4234-4242.
32. Cho YG, Nam SW, Kim TY, Kim YS, Kim CJ, Park JY, Lee JH, Kim HS, Lee JW, Park CH, et al. Overexpression of S100A4 is closely related to the aggressiveness of gastric cancer. Apmis 2003, 111:539-545. 10.1034/j.1600-0463.2003.1110502.x, 12887505.
33. Bertram J, Palfner K, Hiddemann W, Kneba M. Elevated expression of S100P, CAPL and MAGE 3 in doxorubicin-resistant cell lines: comparison of mRNA differential display reverse transcription-polymerase chain reaction and subtractive suppressive hybridization for the analysis of differential gene expression. Anticancer Drugs 1998, 9:311-317. 10.1097/00001813-199804000-00004, 9635921.
34. Kim YJ, Kim MA, Im SA, Kim TM, Kim DW, Yang HK, Heo DS, Lee KU, Choe KJ, Kim NK, et al. Metastasis-associated protein S100A4 and p53 predict relapse in curatively resected stage III and IV (M0) gastric cancer. Cancer Invest 2008, 26:152-158. 10.1080/07357900701518909, 18259945.
35. Arumugam T, Simeone DM, Van Golen K, Logsdon CD. S100P promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res 2005, 11:5356-5364. 10.1158/1078-0432.CCR-05-0092, 16061848.
36. Pedersen KB, Andersen K, Fodstad O, Maelandsmo GM. Sensitization of interferon-gamma induced apoptosis in human osteosarcoma cells by extracellular S100A4. BMC Cancer 2004, 4:52. 10.1186/1471-2407-4-52, 515304, 15318945.
37. Maelandsmo GM, Hovig E, Skrede M, Engebraaten O, Florenes VA, Myklebost O, Grigorian M, Lukanidin E, Scanlon KJ, Fodstad O. Reversal of the in vivo metastatic phenotype of human tumor cells by an anti-CAPL (mts1) ribozyme. Cancer Res 1996, 56:5490-5498.
38. Micale MA, Visscher DW, Gulino SE, Wolman SR. Chromosomal aneuploidy in proliferative breast disease. Hum Pathol 1994, 25:29-35. 10.1016/0046-8177(94)90167-8, 8314258.
39. Pandis N, Heim S, Bardi G, Idvall I, Mandahl N, Mitelman F. Whole-arm t(1;16) and i(1q) as sole anomalies identify gain of 1q as a primary chromosomal abnormality in breast cancer. Genes Chromosomes Cancer 1992, 5:235-238. 10.1002/gcc.2870050310, 1384676.
40. Forus A, Weghuis DO, Smeets D, Fodstad O, Myklebost O, Geurts van Kessel A. Comparative genomic hybridization analysis of human sarcomas: II. Identification of novel amplicons at 6p and 17p in osteosarcomas. Genes Chromosomes Cancer 1995, 14:15-21. 10.1002/gcc.2870140104, 8527379.
41. Nakamura N, Takenaga K. Hypomethylation of the metastasis-associated S100A4 gene correlates with gene activation in human colon adenocarcinoma cell lines. Clin Exp Metastasis 1998, 16:471-479. 10.1023/A:1006589626307, 10091942.
42. Li Y, Zhang KL, Sun Y, Yang Y, Chen XY, Kong QY, Wu ML, Liu J, Li H. Frequent S100A4 Expression with Unique Splicing Pattern in Gastric Cancers: A Hypomethylation Event Paralleled with E-cadherin Reduction and Wnt Activation. Transl Oncol 2008, 1:165-176. 2582165, 19043527.
43. Kohya N, Kitajima Y, Jiao W, Miyazaki K. Effects of E-cadherin transfection on gene expression of a gallbladder carcinoma cell line: repression of MTS1/S100A4 gene expression. Int J Cancer 2003, 104:44-53. 10.1002/ijc.10920, 12532418.
44. Norris MD, De Graaf D, Haber M, Kavallaris M, Madafiglio J, Gilbert J, Kwan E, Stewart BW, Mechetner EB, Gudkov AV, Roninson IB. Involvement of MDR1 P-glycoprotein in multifactorial resistance to methotrexate. Int J Cancer 1996, 65:613-619. 10.1002/(SICI)1097-0215(19960301)65:5<613::AID-IJC10>3.0.CO;2-8, 8598312.
45. Yamada T, Takaoka AS, Naishiro Y, Hayashi R, Maruyama K, Maesawa C, Ochiai A, Hirohashi S. Transactivation of the multidrug resistance 1 gene by T-cell factor 4/beta-catenin complex in early colorectal carcinogenesis. Cancer Res 2000, 60:4761-4766.
46. Berge G, Maelandsmo GM. Evaluation of potential interactions between the metastasis-associated protein S100A4 and the tumor suppressor protein p53. Amino Acids
47. Klingelhofer J, Moller HD, Sumer EU, Berg CH, Poulsen M, Kiryushko D, Soroka V, Ambartsumian N, Grigorian M, Lukanidin EM. Epidermal growth factor receptor ligands as new extracellular targets for the metastasis-promoting S100A4 protein. Febs J 2009, 276:5936-5948. 10.1111/j.1742-4658.2009.07274.x, 19740107.
48. Garrett SC, Varney KM, Weber DJ, Bresnick AR. S100A4, a mediator of metastasis. J Biol Chem 2006, 281:677-680. 10.1074/jbc.R500017200, 16243835.
49. Nakanishi C, Toi M. Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005, 5:297-309. 10.1038/nrc1588, 15803156.
50. Grigorian M, Andresen S, Tulchinsky E, Kriajevska M, Carlberg C, Kruse C, Cohn M, Ambartsumian N, Christensen A, Selivanova G, Lukanidin E. Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction. J Biol Chem 2001, 276:22699-22708. 10.1074/jbc.M010231200, 11278647.
51. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991, 253:49-53. 10.1126/science.1905840, 1905840.
52. Kinsella AR, Smith D, Pickard M. Resistance to chemotherapeutic antimetabolites: a function of salvage pathway involvement and cellular response to DNA damage. Br J Cancer 1997, 75:935-945. 2222738, 9083327.
53. Weller M. Predicting response to cancer chemotherapy: the role of p53. Cell Tissue Res 1998, 292:435-445. 10.1007/s004410051072, 9582400.
54. Liang H, Zhan HJ, Wang BG, Pan Y, Hao XS. Change in expression of apoptosis genes after hyperthermia, chemotherapy and radiotherapy in human colon cancer transplanted into nude mice. World J Gastroenterol 2007, 13:4365-4371.