Induction of metastasis by S100P in a rat mammary model and its association with poor survival of breast cancer patients

Cancer Research

Volumn 66, Issue 2, 2006, Pages 1199-1207

  Wang, Guozheng ^a   Platt Higgins, Angela ^a   Carroll, Joe ^a   De Silva Rudland, Suzete ^a   Winstanley, John ^a   Barraclough, Roger ^a   Rudland, Philip S ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CALCIUM BINDING PROTEIN; CALVASCULIN; OSTEOPONTIN; PROTEIN S 100; PROTEIN S100P; UNCLASSIFIED DRUG;

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER GROWTH; CANCER INVASION; CANCER MODEL; CANCER MORTALITY; CANCER SURVIVAL; CELL CLONE; CONTROLLED STUDY; EXPRESSION VECTOR; FEMALE; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODY FORMATION; BREAST NEOPLASMS; CALCIUM-BINDING PROTEINS; CARCINOMA; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOHISTOCHEMISTRY; MAMMARY NEOPLASMS, ANIMAL; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; OSTEOPONTIN; PROGNOSIS; RATS; RATS, WISTAR; RISK ASSESSMENT; S100 PROTEINS; SIALOGLYCOPROTEINS; SURVIVAL ANALYSIS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 31544449414     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-2605     Document Type: Article

References (43)

1. 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;33:637-68.
2. Zimmer DB, Wright Sadosky P, Weber DJ. Molecular mechanisms of S100-target protein interactions. Microsc Res Tech 2003;60:552-9.
3. Heizmann CW, Fritz G, Schäfer BW. S100 proteins: structure, functions and pathology. Front Biosci 2002; 7:D1356-68.
4. Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 2004;322:1111-22.
5. 2+ binding properties. Eur J Biochem 1992;207:541-7.
6. Crnogorac-Jurcevic T, Missiaglia E, Blaveri E, et al. Molecular alterations in pancreatic carcinoma: expression profiling shows that dysregulated expression of S100 genes is highly prevalent. J Pathol 2003;201: 63-74.
7. Logsdon CD, Simeone DM, Binkley C, et al. Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res 2003;63: 2649-57.
8. Fukushima N, Sato N, Prasad N, Leach SD, Hruban RH, Goggins M. Characterization of gene expression in mucinous cystic neoplasms of the pancreas using oligonucleotide microarrays. Oncogene 2004;23:9042-51.
9. 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 2004;112:100-12.
10. Diederichs S, Bulk E, Steffen B, et al. S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage non-small cell lung cancer. Cancer Res 2004;64:5564-9.
11. Li Y, St. John MA, Zhou X, et al. Salivary transcriptome diagnostics for oral cancer detection. Clin Cancer Res 2004;10:8442-50.
12. Mousses S, Bubendorf L, Wagner U, et al. Clinical validation of candidate genes associated with prostate cancer progression in the CWR22 model system using tissue microarrays. Cancer Res 2002;62:1256-60.
13. da Silva IDG, Hu YF, Russo IH, et al. S100P calcium-binding protein overexpression is associated with immortalization of human breast epithelial cells in vitro and early stages of breast cancer development in vivo. Int J Oncol 2000;16:231-40.
14. Mackay A, Jones C, Dexter T, et al. cDNA microarray analysis of genes associated with ERBB2 (HER2/neu) overexpression in human mammary luminal epithelial cells. Oncogene 2003;22:2680-8.
15. 2+-binding protein S100P. J Mol Biol 2003;325:785-94.
16. Dunnington DJ, Hughes CM, Monaghan P, Rudland PS. Phenotypic instability of rat mammary tumor epithelial cells. J Natl Cancer Inst 1983;71:1227-40.
17. Wang G, Zhang S, Fernig DG, Martin-Fernandez M, Rudland PS, Barraclough R. Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes. Oncogene 2005;24:1445-54.
18. Barraclough R, Kimbell R, Rudland PS. Differential control of mRNA levels for Thy-1 antigen and laminin in rat mammary epithelial and myoepithelial-like cells. J Cell Physiol 1987;131:393-401.
19. Sambrook J, Fritsch EF, Maniatis T. 2nd ed. In: Molecular Cloning: A Laboratory Manual. New York (NY): Cold Spring Harbor Laboratory Press, Cold Spring Harbor; 1989.
20. Rudland PS, Platt-Higgins A, Renshaw C, et al. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 2000;60:1595-603.
21. Wang G, Zhang Z, Fernig DG, et al. Heterodimerisation and the heterodimeric interfaces of S100A1 and S100P. Biochem J 2004;382:375-83.
22. Davies BR, Davies MP, Gibbs FEM, Barraclough R, Rudland PS. Induction of the metastatic phenotype by transfection of a benign rat mammary epithelial cell line with the gene for p9Ka, a rat calcium-binding protein, but not with the oncogene EJ-ras-1. Oncogene 1993;8: 999-1008.
23. Jenkinson SR, Barraclough R, West CR, Rudland PS. S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer 2004;90: 253-62.
24. Rudland PS, Platt-Higgins A, El-Tanani M, et al. Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res 2002;62:3417-27.
25. Platt-Higgins AM, Renshaw CA, West CR, et al. Comparison of the metastasis-inducing protein S100A4 (p9ka) with other prognostic markers in human breast cancer. Int J Cancer 2000;89:198-208.
26. Altman DG. Practical Statistics for Medical Research. London: Chapman and Hall; 1991. p. 403-5.
27. Winstanley J, Cooke T, Murray GD, et al. The long term prognostic significance of c-erbB-2 in primary breast cancer. Br J Cancer 1991;63:447-50.
28. Winstanley JH, Leinster SJ, Cooke TG, Westley BR, Platt-Higgins AM, Rudland PS. Prognostic significance of cathepsin-D in patients with breast cancer. Br J Cancer 1993;67:767-72.
29. Cox DR. Regression models and life tables. J Roy Stat Soc B (Lond) 1972;34:187-202.
30. Oates AJ, Barraclough R, Rudland PS. The identification of osteopontin as a metastasis-related gene product in a rodent mammary tumour model. Oncogene 1996;13: 97-104.
31. Zhang S, Wang G, Liu D, et al. The C-terminal region of S100A4 is important for its metastasis-inducing properties. Oncogene 2005;24:4401-11.
32. Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R. Human homologue of cement gland protein, a novel metastasis inducer associated with breast carcinomas. Cancer Res 2005;65:3796-805.
33. Kerbel RS, Waghorne C, Man MS, Elliott B, Breitman ML. Alteration of the tumorigenic and metastatic properties of neoplastic cells is associated with the process of calcium phosphate-mediated DNA transfection. Proc Natl Acad Sci U S A 1987;84:1263-7.
34. 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;9:311-7.
35. Lloyd BH, Platt-Higgins A, Rudland PS, Barraclough R. Human S100A4 (p9Ka) induces the metastatic phenotype on benign tumour cells. Oncogene 1998;17: 465-73.
36. Mueller A, Bachi T, Hochli M, Schäfer BW, Heizmann CW. Subcellular distribution of S100 proteins in tumor cells and their relocation in response to calcium activation. Histochem Cell Biol 1999;111: 453-9.
37. Mandinova A, Atar D, Schäfer BW, Spiess M, Aebi U, Heizmann CW. Distinct subcellular localization of calcium binding S100 proteins in human smooth muscle cells and their relocation in response to rises in intracellular calcium. J Cell Sci 1998;111:2043-54.
38. Sorci G, Bianchi R, Giambanco I, Rambotti MG, Donate R. Replicating myoblasts and fused myotubes express the calcium-regulated proteins S100A1 and S100B. Cell Calcium 1999;25:93-106.
39. Rudland PS, Platt-Higgins AM, Wilkinson MC, Fernig DG. Immunocytochemical identification of basic fibroblast growth factor in the developing rat mammary gland: variations in location are dependent on glandular structure and differentiation. J Histochem Cytochem 1993;41:887-98.
40. Ambartsumian N, Klingelhofer J, Grigorian M, et al. The metastasis-associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 2001;20: 4685-95.
41. Schmidt-Hansen B, Klingelhofer J, Grum-Schwensen B, et al. Functional significance of metastasis-inducing S100A4(Mts1) in tumor-stroma interplay. J Biol Chem 2004;279:24498-504.
42. van de Vijver MJ, He YD, van't Veer LJ, et al. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002;347:1999-2009.
43. Vallely KM, Rustandi RR, Ellis KC, Varlamova O, Bresnick AR, Weber DJ. Solution structure of human Mts1 (S100A4) as determined by NMR spectroscopy. Biochemistry 2002;41:12670-80.