S100A4-induced cell motility and metastasis is restricted by the Wnt/β-catenin pathway inhibitor calcimycin in colon cancer cells

Molecular Biology of the Cell

Volumn 22, Issue 18, 2011, Pages 3344-3354

  Sack, Ulrike ^a   Walther, Wolfgang ^b   Scudiero, Dominic ^c   Selby, Mike ^c   Aumann, Jutta ^a   Lemos, Clara ^a   Fichtner, Iduna ^a   Schlag, Peter M ^a,b   Shoemaker, Robert H ^d   Stein, Ulrike ^b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c SAIC FREDERICK INC   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CALCIMYCIN; CALVASCULIN; CYCLIN D1; DICKKOPF 1 PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; MYC PROTEIN; WNT PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; GENE EXPRESSION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CALCIMYCIN; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; GENE EXPRESSION; GENES, REPORTER; HCT116 CELLS; HUMANS; LIVER NEOPLASMS; LUCIFERASES; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; PROMOTER REGIONS, GENETIC; S100 PROTEINS; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 80052823397     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-09-0739     Document Type: Article

References (46)

1. Ambartsumian N et al. (2001). The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 20, 4685-4695.
2. Ambartsumian NS, Grigorian MS, Larsen IF, Karlstrom O, Sidenius N, Rygaard J, Georgiev G, Lukanidin E (1996). Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene. Oncogene 13, 1621-1630.
3. Amit S, Hatzubai A, Birman Y, Andersen JS, Ben-Shushan E, Mann M, Ben-Neriah Y, Alkalay I (2002). Axin-mediated CKI phosphorylation of beta-catenin at Ser 45: a molecular switch for the Wnt pathway. Genes Dev 16, 1066-1076.
4. Barker N, Clevers H (2006). Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov 5, 997-1014.
5. Becker M, Nitsche A, Neumann C, Aumann J, Junghahn I, Fichtner I (2002). Sensitive PCR method for the detection and real-time quantification of human cells in xenotransplantation systems. Br J Cancer 87, 1328-1335.
6. Belot N, Pochet R, Heizmann CW, Kiss R, Decaestecker C (2002). Extracellular S100A4 stimulates the migration rate of astrocytic tumor cells by modifying the organization of their actin cytoskeleton. Biochim Biophys Acta 1600, 74-83.
7. Boyden S (1962). The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leucocytes. J Exp Med 115, 453-466.
8. Boye K, Maelandsmo GM (2010). S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176, 528-535.
9. Cho YG, Kim CJ, Nam SW, Yoon SH, Lee SH, Yoo NJ, Lee JY, Park WS (2005). Overexpression of S100A4 is closely associated with progression of colorectal cancer. World J Gastroenterol 11, 4852-4856.
10. Davies MP, Rudland PS, Robertson L, Parry EW, Jolicoeur P, Barraclough R (1996). Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours. Oncogene 13, 1631-1637.
11. Engelkamp D, Schafer BW, Erne P, Heizmann CW (1992). S100 alpha, CAPL, and CACY: molecular cloning and expression analysis of three calcium-binding proteins from human heart. Biochemistry 31, 10258-10264.
12. Ford HL, Silver DL, Kachar B, Sellers JR, Zain SB (1997). Effect of Mts1 on the structure and activity of nonmuscle myosin II. Biochemistry 36, 16321-16327.
13. Gao XN, Tang SQ, Zhang XF (2005). S100A4 antisense oligodeoxynucleotide suppresses invasive potential of neuroblastoma cells. J Pediatr Surg 40, 648-652.
14. Garrett SC, Varney KM, Weber DJ, Bresnick AR (2006). S100A4, a mediator of metastasis. J Biol Chem 281, 677-680.
15. Giles RH, van Es JH, Clevers H (2003). Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 1653, 1-24.
16. Gongoll S, Peters G, Mengel M, Piso P, Klempnauer J, Kreipe H, von Wasielewski R (2002). Prognostic significance of calcium-binding protein S100A4 in colorectal cancer. Gastroenterology 123, 1478-1484.
17. Gonzalez-Sancho JM, Aguilera O, Garcia JM, Pendas-Franco N, Pena C, Cal S, Garcia de Herreros A, Bonilla F, Munoz A (2005). The Wnt antagonist DICKKOPF-1 gene is a downstream target of beta-catenin/TCF and is downregulated in human colon cancer. Oncogene 24, 1098-1103.
18. Grigorian M, Tulchinsky E, Burrone O, Tarabykina S, Georgiev G, Lukanidin E (1994). Modulation of mts1 expression in mouse and human normal and tumor cells. Electrophoresis 15, 463-468.
19. Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E, Ambartsumian N (2005). Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65, 3772-3780.
20. Gwak J et al. (2006). Protein-kinase-C-mediated beta-catenin phosphorylation negatively regulates the Wnt/beta-catenin pathway. J Cell Sci 119, 4702-4709.
21. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW (1998). Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
22. Hernan R, Fasheh R, Calabrese C, Frank AJ, Maclean KH, Allard D, Barraclough R, Gilbertson RJ (2003). ERBB2 up-regulates S100A4 and several other prometastatic genes in medulloblastoma. Cancer Res 63, 140-148.
23. Hua J, Chen D, Fu H, Zhang R, Shen W, Liu S, Sun K, Sun X (2009). Short hairpin RNA-mediated inhibition of S100A4 promotes apoptosis and suppresses proliferation of BGC823 gastric cancer cells in vitro and in vivo. Cancer Lett 292, 41-47.
24. Huang WS, Wang JP, Wang T, Fang JY, Lan P, Ma JP (2007). ShRNA-mediated gene silencing of beta-catenin inhibits growth of human colon cancer cells. World J Gastroenterol 13, 6581-6587.
25. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ (2008). Cancer statistics, 2008. CA Cancer J Clin 58, 71-96.
26. Keirsebilck A, Bonne S, Bruyneel E, Vermassen P, Lukanidin E, Mareel M, van Roy F (1998). E-cadherin and metastasin (mts-1/S100A4) expression levels are inversely regulated in two tumor cell families. Cancer Res 58, 4587-4591.
27. Kim EJ, Helfman DM (2003). Characterization of the metastasis-associated protein, S100A4Roles of calcium binding and dimerization in cellular localization and interaction with myosin. J Biol Chem 278, 30063-30073.
28. Kim JS, Crooks H, Dracheva T, Nishanian TG, Singh B, Jen J, Waldman T (2002). Oncogenic beta-catenin is required for bone morphogenetic protein 4 expression in human cancer cells. Cancer Res 62, 2744-2748.
29. Kriajevska M, Fischer-Larsen M, Moertz E, Vorm O, Tulchinsky E, Grigorian M, Ambartsumian N, Lukanidin E (2002). Liprin beta 1, a member of the family of LAR transmembrane tyrosine phosphatase-interacting proteins, is a new target for the metastasis-associated protein S100A4 (Mts1). J Biol Chem 277, 5229-5235.
30. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP, Lukanidin EM (1994). Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269, 19679-19682.
31. Li ZH, Bresnick AR (2006). The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res 66, 5173-5180.
32. Li ZH, Spektor A, Varlamova O, Bresnick AR (2003). Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42, 14258-14266.
33. Mathisen B, Lindstad RI, Hansen J, El-Gewely SA, Maelandsmo GM, Hovig E, Fodstad O, Loennechen T, Winberg JO (2003). S100A4 regulates membrane induced activation of matrix metalloproteinase-2 in osteosarcoma cells. Clin Exp Metastasis 20, 701-711.
34. Pressman BC (1976). Biological applications of ionophores. Annu Rev Biochem 45, 501-530.
35. Rapisarda A, Uranchimeg B, Scudiero DA, Selby M, Sausville EA, Shoemaker RH, Melillo G (2002). Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 62, 4316-4324.
36. Sack U, Stein U (2009). Wnt up your mind-intervention strategies for S100A4-induced metastasis in colon cancer. Gen Physiol Biophys 28, F55-F64.
37. Saleem M et al. (2006). S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA 103, 14825-14830.
38. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006). Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 396, 201-214.
39. Schneider M, Hansen JL, Sheikh SP (2008). S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J Mol Med 86, 507-522.
40. Sherbet GV (2009). Metastasis promoter S100A4 is a potentially valuable molecular target for cancer therapy. Cancer Lett 280, 15-30.
41. Shi Y, Zou M, Collison K, Baitei EY, Al-Makhalafi Z, Farid NR, Al-Mohanna FA (2006). Ribonucleic acid interference targeting S100A4 (Mts1) suppresses tumor growth and metastasis of anaplastic thyroid carcinoma in a mouse model. J Clin Endocrinol Metab 91, 2373-2379.
42. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A (1999). The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 96, 5522-5527.
43. Stein U, Arlt F, Smith J, Sack U, Herrmann P, Walther W, Lemm M, Fichtner I, Shoemaker RH, Schlag PM (2011). Intervening in β-catenin signaling by sulindac inhibits S100A4-dependent colon cancer metastasis. Neoplasia 13, 131-144.
44. Stein U et al. (2006). The metastasis-associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 131, 1486-1500.
45. Tabata T et al. (2009). RNA interference targeting against S100A4 suppresses cell growth and motility and induces apoptosis in human pancreatic cancer cells. Biochem Biophys Res Commun 390, 475-480.
46. Yammani RR, Carlson CS, Bresnick AR, Loeser RF (2006). Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: Role of the receptor for advanced glycation end products. Arthritis Rheum 54, 2901-2911.