Identification of a key molecular regulator of liver metastasis in human pancreatic carcinoma using a novel quantitative model of metastasis in NOD/SCID/γc null (NOG) mice

International Journal of Oncology

Volumn 31, Issue 4, 2007, Pages 741-751

  Suemizu, Hiroshi ^a   Monnai, Makoto ^a,b   Ohnishi, Yasuyuki ^a   Ito, Mamoru ^a   Tamaoki, Norikazu ^a   Nakamura, Masato ^a,c,d  

^a CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^b Chugai Research Institute   (Japan)

^c TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d TOKAI UNIVERSITY HACHIOJI HOSPITAL   (Japan)

Author keywords

Human pancreatic cancer; Liver metastasis; NOG mice

Indexed keywords

PROTEIN S 100; RNA; S100A4 PROTEIN, MOUSE; TUMOR MARKER; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; CELL CULTURE; DISEASE MODEL; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIVER TUMOR; MALE; METABOLISM; METASTASIS; MOUSE; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, NEOPLASM; S100 PROTEINS; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 35848931900     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.31.4.741     Document Type: Article

References (49)

1. Fidler IJ: The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3: 453-458, 2003.
2. Giavazzi R, Campbell DE, Jessup JM, Cleary K and Fidler IJ: Metastatic behavior of tumor cells isolated from primary and metastatic human colorectal carcinomas implanted into different sites in nude mice. Cancer Res 46: 1928-1933, 1986.
3. Ikeda Y, Ezaki M, Hayashi I, Yasuda D, Nakayama K and Kono A: Establishment and characterization of human pancreatic cancer cell lines in tissue culture and in nude mice. Jpn J Cancer Res 81: 987-993, 1990. (Pubitemid 20336591)
4. Kuo TH, Kubota T, Nishibori H, et al: Experimental cancer chemotherapy using a liver metastatic model of human colon cancer transplanted into the spleen of severe combined immunodeficient mice. J Surg Oncol 52: 92-96, 1993. (Pubitemid 23061956)
5. Ohbo K, Suda T, Hashiyama M, et al: Modulation of hematopoiesis in mice with a truncated mutant of the interleukin-2 receptor gamma chain. Blood 87: 956-967, 1996. (Pubitemid 26043526)
6. Koyanagi Y, Tanaka Y, Kira J, et al: Primary human immunodeficiency virus type 1 viremia and central nervous system invasion in a novel hu-PBL-immunodeficient mouse strain. J Virol 71: 2417-2424, 1997. (Pubitemid 27078625)
7. Ito M, Hiramatsu H, Kobayashi K, et al: NOD/SCID/ gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 100: 3175-3182, 2002. (Pubitemid 35217065)
8. null (NOG) mouse model. Oncol Rep 14: 633-637, 2005.
9. Khatib AM, Fallavollita L, Wancewicz EV, Monia BP and Brodt P: Inhibition of hepatic endothelial E-selectin expression by C-raf antisense oligonucleotides blocks colorectal carcinoma liver metastasis. Cancer Res 62: 5393-5398, 2002.
10. Jain N, Thatte J, Braciale T, Ley K, O'Connell M and Lee JK: Local-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays. Bioinformatics 19: 1945-1951, 2003.
11. Niwa H, Yamamura K and Miyazaki J: Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199, 1991.
12. Missiaglia E, Blaveri E, Terris B, et al: Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int J Cancer 112: 100-112, 2004. (Pubitemid 39249497)
13. Han H, Bearss DJ, Browne LW, Calaluce R, Nagle RB and Von Hoff DD: Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res 62: 2890-2896, 2002. Erratum in: Cancer Res 62: 4532, 2002.
14. Ryu B, Jones J, Blades NJ, Parmigiani G, Hollingsworth MA, Hruban RH and Kern SE: Relationships and differentially expressed genes among pancreatic cancers examined by large-scale serial analysis of gene expression. Cancer Res 62: 819-826, 2002. (Pubitemid 34126959)
15. Bresalier RS, Raper SE, Hujanen ES and Kim YS: A new animal model for human colon cancer metastasis. Int J Cancer 39: 625-630, 1987.
16. Nicholson BE, Frierson HF, Conaway MR, Seraj JM, Harding MA, Hampton GM and Theodorescu D: Profiling the evolution of human metastatic bladder cancer. Cancer Res 64: 7813-7821, 2004.
17. Nishimori H, Yasoshima T, Hata F, et al: A novel nude mouse model of liver metastasis and peritoneal dissemination from the same human pancreatic cancer line. Pancreas 24: 242-250, 2002.
18. Shishido T, Yasoshima T, Hirata K, et al: Establishment and characterization of human pancreatic carcinoma lines with a high metastatic potential in the liver of nude mice. Surg Today 29: 519-525, 1999.
19. Nomura H, Nishimori H, Yasoshima T, et al: A new liver metastatic and peritoneal dissemination model established from the same human pancreatic cancer cell line: analysis using cDNA macroarray. Clin Exp Metastasis 19: 391-399, 2002.
20. Gildea JJ, Golden WL, Harding MA and Theodorescu D: Genetic and phenotypic changes associated with the acquisition of tumorigenicity in human bladder cancer. Genes Chromosomes Cancer 27: 252-263, 2000.
21. Park KJ and Kanehisa M: Prediction of protein subcellular locations by support vector machines using compositions of amino acids and amino acid pairs. Bioinformatics 19: 1656-1663, 2003.
22. Dokmanovic M, Chang BD, Fang J and Roninson IB: Retinoid-induced growth arrest of breast carcinoma cells involves coactivation of multiple growth-inhibitory genes. Cancer Biol Ther 1: 24-27, 2002.
23. Lee JH and Welch DR: Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer Res 57: 2384-2387, 1997.
24. Hosono K, Sasaki T, Minoshima S and Shimizu N: Identification and characterization of a novel gene family YPEL in a wide spectrum of eukaryotic species. Gene 340: 31-43, 2004.
25. Heizmann CW, Fritz G and Schafer BW: S100 proteins: structure, functions and pathology. Front Biosci 7: d1356-d1368, 2002.
26. Davies BR, O'Donnell M, Durkan GC, Rudland PS, Barraclough R, Neal DE and Mellon JK: Expression of S100A4 protein is associated with metastasis and reduced survival in human bladder cancer. J Pathol 196: 292-299, 2002.
27. Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L and Barraclough R: Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 60: 1595-1603, 2000. (Pubitemid 30183430)
28. Takenaga K, Nakanishi H, Wada K, Suzuki M, Matsuzaki O, Matsuura A and Endo H: Increased expression of S100A4, a metastasis-associated gene, in human colorectal adenocarcinomas. Clin Cancer Res 3: 2309-2316, 1997.
29. Yonemura Y, Endou Y, Kimura K, et al: Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 6: 4234-4242, 2000.
30. Grigorian M, Ambartsumian N, Lykkesfeldt AE, Bastholm L, Elling F, Georgiev G and Lukanidin E: Effect of mts1 (S100A4) expression on the progression of human breast cancer cells. Int J Cancer 67: 831-841, 1996.
31. Lloyd BH, Platt-Higgins A, Rudland PS and Barraclough R: Human S100A4 (p9Ka) induces the metastatic phenotype upon benign tumour cells. Oncogene 17: 465-473, 1998.
32. Levett D, Flecknell PA, Rudland PS, Barraclough R, Neal DE, Mellon JK and Davies BR: Transfection of S100A4 produces metastatic variants of an orthotopic model of bladder cancer. Am J Pathol 160: 693-700, 2002.
33. Maelandsmo GM, Hovig E, Skrede M, et al: Reversal of the in vivo metastatic phenotype of human tumor cells by an anti-CAPL (mts1) ribozyme. Cancer Res 56: 5490-5498, 1996.
34. Bjornland K, Winberg JO, Odegaard OT, et al: S100A4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-S100A4 ribozyme. Cancer Res 59: 4702-4708, 1999.
35. Takenaga K, Nakamura Y and 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 14: 331-337, 1997.
36. Yanagihara K, Seyama T and Watanabe Y: Antitumor potential of interferon-gamma: retroviral expression of mouse interferon-gamma cDNA in two kinds of highly metastatic mouse tumor lines reduces their tumorigenicity. Nat Immun 13: 102-112, 1994.
37. Takenaga K: Suppression of metastasis-associated S100A4 gene expression by gamma-interferon in human colon adenocarcinoma cells. Br J Cancer 80: 127-132, 1999.
38. Andersen K, Smith-Sorensen B, Pedersen KB, Hovig E, Myklebost O, Fodstad O and Maelandsmo GM: Interferon-gamma suppresses S100A4 transcription independently of apoptosis or cell cycle arrest. Br J Cancer 88: 1995-2001, 2003.
39. Hernan R, Fasheh R, Calabrese C, et al: ERBB2 up-regulates S100A4 and several other prometastatic genes in medulloblastoma. Cancer Res 63: 140-148, 2003.
40. Rosty C, Ueki T, Argani P, et al: Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol 160: 45-50, 2002.
41. Chen D, Rudland PS, Chen HL and Barraclough R: Differential reactivity of the rat S100A4(p9Ka) gene to sodium bisulfite is associated with differential levels of the S100A4 (p9Ka) mRNA in rat mammary epithelial cells. J Biol Chem 274: 2483-2491, 1999.
42. Sato N, Maitra A, Fukushima N, et al: Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 63: 4158-4166, 2003.
43. Zingg JM and Jones PA: Genetic and epigenetic aspects of DNA methylation on genome expression, evolution, mutation and carcinogenesis. Carcinogenesis 18: 869-882, 1997.
44. Counts JL and Goodman JI: Alterations in DNA methylation may play a variety of roles in carcinogenesis. Cell 83: 13-15, 1995.
45. Engelkamp D, Schafer BW, Mattei MG, Erne P and Heizmann CW: Six S100 genes are clustered on human chromosome 1q21: identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E. Proc Natl Acad Sci USA 90: 6547-6551, 1995.
46. Meza-Zepeda LA, Forus A, Lygren B, et al: Positional cloning identifies a novel cyclophilin as a candidate amplified oncogene in 1q21. Oncogene 21: 2261-2269, 2002.
47. Kudoh K, Takano M, Koshikawa T, et al: Gains of 1q21-q22 and 13q12-q14 are potential indicators for resistance to cisplatin-based chemotherapy in ovarian cancer patients. Clin Cancer Res 5: 2526-2531, 1999.
48. Wong N, Chan A, Lee SW, et al: Positional mapping for amplified DNA sequences on 1q21-q22 in hepatocellular carcinoma indicates candidate genes over-expression. J Hepatol 38: 298-306, 2003.
49. Gronwald J, Storkel S, Holtgreve-Grez H, et al: Comparison of DNA gains and losses in primary renal clear cell carcinomas and metastatic sites: importance of 1q and 3p copy number changes in metastatic events. Cancer Res 57: 481-487, 1997.