Abstract
Increased levels of the homodimeric calcium-binding protein, S100A4, have been shown to cause a metastatic phenotype in at least three independent model systems of breast cancer and its presence in carcinoma cells has been shown to be associated with a reduction in the survival of patients suffering from a range of different cancers. S100A4 has been shown to interact in vitro with another member of the S100 family of proteins, S100A1. The purpose of the present study was to find out whether S100A1 could affect S100A4 function. Fluorescence resonance energy transfer was used to show the interaction of S100A4 and S100A1 in living cells and the binding affinities between S100A4 and S100A1 were determined using a biosensor. S100A1 reduced the S100A4 inhibition of nonmuscle myosin A self-association and phosphorylation in vitro. S100A1 reduced S100A4 induced motility and growth in soft agar and metastasis in vivo. The results show for the first time that interactions between different S100 proteins can affect cancer-related activity, and that the presence of S100A1 protein in carcinoma cells might modulate the effect of S100A4 on their metastatic abilities.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 50 print issues and online access
$259.00 per year
only $5.18 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Ambartsumian N, Grigorian M, Larsen F, Karlstrom O, Sidenius N, Rygaard J, Georgiev G and Lukanidin E . (1996). Oncogene, 13, 1621–1630.
Becker D and Fikes J . (1993). Gene Transcription, A Practical Approach: Hames B and Higgins S (eds). IRL Press: Oxford, pp 295–319.
Chen H-L, Fernig DG, Rudland PS, Sparks A, Wilkinson MC and Barraclough R . (2001). Biochem. Biophys. Res. Commun., 286, 1212–1217.
Davies BR, Davies MPA, Gibbs FEM, Barraclough R and Rudland PS . (1993). Oncogene, 8, 999–1008.
Davies BR, O'Donnell M, Durkan GC, Rudland PS, Barraclough R, Neal DE and Mellon JK . (2002). J. Pathol., 196, 292–299.
Davies MPA, Rudland PS, Robertson L, Parry EW, Jolicoeur PS and Barraclough R . (1996). Oncogene, 13, 1631–1637.
Donato R . (2001). Int. J. Biochem. Cell. Biol., 33, 637–668.
Dunnington DJ, Monaghan P, Hughes CM and Rudland PS . (1983). J. Natl. Cancer Inst., 71, 1227–1240.
Endo H, Takenaga K, Kanno T, Satoh H and Mori S . (2002). J. Biol. Chem., 277, 26396–26402.
Ford H and Zain S . (1995). Oncogene, 10, 1597–1605.
Gibbs FEM, Wilkinson MC, Rudland PS and Barraclough R . (1994). J. Biol. Chem., 269, 18992–18999.
Gongoll S, Peters G, Mengel M, Piso P, Klempnauer J, Kreipe H and von Wasielewski R . (2002). Gastroenterology, 123, 1478–1484.
Grigorian M, Andresen S, Tulchinsky E, Kriajevska M, Carlberg C, Kruse C, Cohn M, Ambartsumian N, Christensen A, Selivanova G and Lukanidin E . (2001). J. Biol. Chem., 276, 22699–22708.
Jenkinson SR, Barraclough R, West CR and Rudland PS . (2004). Br. J. Cancer, 90, 253–262.
Kimura K, Endo Y, Yonemura Y, Heizmann C, Schäfer B, Watanabe Y and Sasaki T . (2000). Int. J. Oncol., 16, 1125–1131.
Kriajevska M, Bronstein IB, Scott DJ, Tarabykina S, Fischer-Larsen M, Issinger O and Lukanidin E . (2000). Biochim. Biophys. Acta, 1498, 252–263.
Kriajevska M, Cardenas M, Grigorian M, Ambartsumian N, Georgiev G and Lukanidin E . (1994). J. Biol. Chem., 269, 19679–19682.
Kriajevska M, Fischer-Larsen M, Moertz E, Vorm O, Tulchinsky E, Grigorian M, Ambartsumian N and Lukanidin E . (2002). J. Biol. Chem., 277, 5229–5235.
Kriajevska M, Tarabykina S, Bronstein I, Maitland N, Lomonosov M, Hansen K, Georgiev G and Lukanidin E . (1998). J. Biol. Chem., 273, 9852–9856.
Laemmli UK . (1970). Nature, 227, 680–685.
Lloyd B, Platt-Higgins A, Rudland PS and Barraclough R . (1998). Oncogene, 17, 465–473.
Most P, Bernotat J, Ehlermann P, Pleger ST, Reppel M, Borries M, Niroomand F, Pieske B, Janssen PM, Eschenhagen T, Karczewski P, Smith GL, Koch WJ, Katus HA and Remppis A . (2001). Proc. Natl Acad. Sci. USA, 98, 13889–13894.
Most P, Remppis A, Pleger ST, Loffler E, Ehlermann P, Bernotat J, Kleuss C, Heierhorst J, Ruiz P, Witt H, Karczewski P, Mao L, Rockman HA, Duncan SJ, Katus HA and Koch WJ . (2003). J. Biol. Chem., 278, 33809–33817.
Murakami N, Singh S, Chauhan V and Elzinga M . (1995). Biochemistry, 34, 16046–16055.
Nakamura T, Ajiki T, Murao S, Kamigaki T, Maeda S, Ku Y and Kuroda Y . (2002). Int. J. Oncol., 20, 937–941.
Nakanishi K, Sakamoto M, Yasuda J, Takamura M, Fujita N, Tsuruo T, Todo S and Hirohashi S . (2002). Cancer Res., 62, 2971–2975.
Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, Fujimura T, Nishimura G, Tani T, Shimizu K, Yonemura Y, Heizmann CW, Schäfer B, Sasaki T and Miwa K . (2001). Int. J. Oncol., 18, 715–720.
Pepperkok R, Squire A, Geley S and Bastiaens PI . (1999). Curr. Biol., 9, 269–272.
Rahmoune H, Chen HL, Gallagher JT, Rudland PS and Fernig DG . (1998a). J. Biol. Chem., 273, 7303–7310.
Rahmoune H, Rudland PS, Gallagher JT and Fernig DG . (1998b). Biochemistry, 37, 6003–6008.
Rudland PS, Dunnington DJ, Gusterson B, Monaghan P and Hughes CM . (1984). Cancer Res., 44, 2089–2101.
Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JHR, Robertson L and Barraclough R . (2000). Cancer Res., 60, 1595–1603.
Rustandi RR, Baldisseri DM, Inman KG, Nizner P, Hamilton SM, Landar A, Zimmer DB and Weber DJ . (2002). Biochemistry, 41, 788–796.
Sambrook J, Fritsch EF and Maniatis T . (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
Selinfreund RH, Barger SW, Pledger WJ and Van Eldik LJ . (1991). Proc. Natl. Acad. Sci. USA, 88, 3554–3558.
Sorci G, Bianchi R, Giambanco I, Rambotti MG and Donato R . (1999). Cell Calcium, 25, 93–106.
Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K and Endo H . (1994). J. Cell Biol., 124, 757–768.
Tarabykina S, Kriajevska M, Scott DJ, Hill TJ, Lafitte D, Derrick PJ, Dodson GG, Lukanidin E and Bronstein I . (2000). FEBS Lett., 475, 187–191.
Tarabykina S, Scott DJ, Herzyk P, Hill TJ, Tame JR, Kriajevska M, Lafitte D, Derrick PJ, Dodson GG, Maitland NJ, Lukanidin EM and Bronstein IB . (2001). J. Biol. Chem., 276, 24212–24222.
Vallely KM, Rustandi RR, Ellis KC, Varlamova O, Bresnick AR and Weber DJ . (2002). Biochemistry, 41, 12670–12680.
Wang G, Rudland PS, White MRH and Barraclough R . (2000). J. Biol. Chem., 275, 11141–11146.
Wang G, Zhang S, Fernig DG, Spiller D, Martin-Fernandez M, Zhang H, Ding Y, Rao Z, Rudland PS and Barraclough R . (2004). Biochem. J., 382, 375–383.
Zhang S, Wang G, Fernig DG, Rudland PS, Webb SE, Barraclough R and Martin-Fernandez M . (2004). Eur. Biophys. J., DOI: 10.1007/s00249-004-0428-x (in press).
Acknowledgements
We thank Angela Platt-Higgins for histology and Joe Carroll for excellent technical assistance. This work was supported by the North West Cancer Research Fund, The Cancer and Polio Research Fund and the Biotechnology and Biological Sciences Research Council of the UK.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, G., Zhang, S., Fernig, D. et al. Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes. Oncogene 24, 1445–1454 (2005). https://doi.org/10.1038/sj.onc.1208291
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/sj.onc.1208291
Keywords
This article is cited by
-
Elevated extracellular matrix protein 1 in circulating extracellular vesicles supports breast cancer progression under obesity conditions
Nature Communications (2024)
-
Functional interaction between S100A1 and MDM2 may modulate p53 signaling in normal and malignant endometrial cells
BMC Cancer (2022)
-
Distinct prognostic values of S100 mRNA expression in breast cancer
Scientific Reports (2017)
-
Joining S100 proteins and migration: for better or for worse, in sickness and in health
Cellular and Molecular Life Sciences (2014)
-
S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence
Cancer and Metastasis Reviews (2012)