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Biological Chemistry

Editor-in-Chief: Brüne, Bernhard

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Volume 398, Issue 10

Issues

S100A6 – focus on recent developments

Wiesława Leśniak
  • Laboratory of Calcium Binding Proteins, Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Tomasz Wilanowski
  • Laboratory of Signal Transduction, Department of Cell Biology, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 02-093 Warsaw, Poland
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Anna Filipek
  • Corresponding author
  • Laboratory of Calcium Binding Proteins, Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-03-25 | DOI: https://doi.org/10.1515/hsz-2017-0125

Abstract

The Ca2+-binding protein, S100A6, belongs to the S100 family. Binding of Ca2+ induces a conformational change, which causes an increase in the overall S100A6 hydrophobicity and allows it to interact with many targets. S100A6 is expressed in different normal tissues and in many tumors. Up to now it has been shown that S100A6 is involved in cell proliferation, cytoskeletal dynamics and tumorigenesis, and that it might have some extracellular functions. In this review, we summarize novel discoveries concerning S100A6 targets, its involvement in cellular signaling pathways, and presence in stem/progenitor cells, extracellular matrix and body fluids of diseased patients.

Keywords: body fluids; pathology; S100A6 (calcyclin); S100 family; stem/progenitor cells; tumor

References

  • Acosta, S., Mayol, G., Rodríguez, E., Lavarino, C., de Preter, K., Kumps, C., Garcia, I., de Torres, C., and Mora, J. (2011). Identification of tumoral glial precursor cells in neuroblastoma. Cancer Lett. 312, 73–81.CrossrefPubMedGoogle Scholar

  • Bartkowska, K., Swiatek, I., Aniszewska, A., Jurewicz, E., Turlejski, K., Filipek, A., and Djavadian, R.L. (2017). Stress-dependent changes in the CacyBP/SIP interacting protein S100A6 in the mouse brain. PLoS One 12, e0169760.PubMedCrossrefGoogle Scholar

  • Belt, E.J., Fijneman, R.J., van den Berg, E.G., Bril, H., Delis-van Diemen, P.M., Tijssen, M., van Essen, H.F., de Lange-de Klerk, E.S., Belien, J.A., Stockmann, H.B,, et al. (2011). Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence. Eur. J. Cancer 47, 1837–1845.CrossrefPubMedGoogle Scholar

  • Bresnick, A.R., Weber, D.J., and Zimmer, D.B. (2015). S100 proteins in cancer. Nat. Rev. Cancer 15, 96–109.PubMedCrossrefGoogle Scholar

  • Cai, X.Y., Lu, L., Wang, Y.N., Jin, C., Zhang, R.Y., Zhang, Q., Chen, Q.J., and Shen, W.F. (2011). Association of increased S100B, S100A6 and S100P in serum levels with acute coronary syndrome and also with the severity of myocardial infarction in cardiac tissue of rat models with ischemia-reperfusion injury. Atherosclerosis 217, 536–542.CrossrefPubMedGoogle Scholar

  • Capra, E., Beretta, R., Parazzi, V., Viganò, M., Lazzari, L., Baldi, A., and Giordano, R. (2012). Changes in the proteomic profile of adipose tissue-derived mesenchymal stem cells during passages. Proteome Sci. 10, 46.CrossrefPubMedGoogle Scholar

  • Chen, H., Xu, C., Jin, Q., and Liu, Z. (2014). S100 protein family in human cancer. Am. J. Cancer Res. 4, 89–115.PubMedGoogle Scholar

  • Chen, X., Liu, X., Lang, H., Zhang, S., Luo, Y., and Zhang, J. (2015). S100 calcium-binding protein A6 promotes epithelial-mesenchymal transition through β-catenin in pancreatic cancer cell line. PLoS One 10, e0121319.CrossrefPubMedGoogle Scholar

  • Deloulme, J.C., Assard, N., Mbele, G.O., Mangin, C., Kuwano, R., and Baudier, J. (2000). S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J. Biol. Chem. 275, 35302–35310.CrossrefPubMedGoogle Scholar

  • Donato, R., Cannon, B.R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D.J., and Geczy, C.L. (2013). Functions of S100 proteins. Curr. Mol. Med. 13, 24–57.CrossrefPubMedGoogle Scholar

  • Duan, L., Wu, R., Zou, Z., Wang, H., Ye, L., Li, H., Yuan, S., Li, X, Zha, H., Sun, H., et al. (2014). S100A6 stimulates proliferation and migration of colorectal carcinoma cells through activation of the MAPK pathways. Int. J. Oncol. 44, 781–790.PubMedCrossrefGoogle Scholar

  • Fernandez-Fernandez, M.R., Rutherford, T.J., and Fersht, A.R. (2008) Members of the S100 family bind p53 in two distinct ways. Protein Sci. 17, 1663–1670.CrossrefPubMedGoogle Scholar

  • Filipek, A., Heizmann, C.W., and Kuźnicki, J. (1990). Calcyclin is a calcium and zinc binding protein. FEBS Lett. 264, 263–266.PubMedCrossrefGoogle Scholar

  • Filipek, A., Michowski, W., and Kuznicki, J. (2008) Involvement of S100A6 (calcyclin) and its binding partners in intracellular signaling pathways. Adv. Enzyme Regul. 48, 225–239.CrossrefPubMedGoogle Scholar

  • Fritz, G., Botelho, H.M., Morozova-Roche, L.A., and Gomes, C.M. (2010). Natural and amyloid self-assembly of S100 proteins: structural basis of functional diversity. FEBS J. 277, 4578–4590.CrossrefPubMedGoogle Scholar

  • Góral, A., Bieganowski, P., Prus, W., Krzemień-Ojak Ł., Kądziołka, B., Fabczak, H., and Filipek, A. (2016). Calcyclin binding protein/Siah-1 interacting protein is a Hsp90 binding chaperone. PLoS One 11, e0156507.CrossrefPubMedGoogle Scholar

  • Graczyk, A., Słomnicki, L.P., and Leśniak, W. (2013). S100A6 competes with the TAZ2 domain of p300 for binding to p53 and attenuates p53 acetylation. J. Mol. Biol. 425, 3488–3494.PubMedCrossrefGoogle Scholar

  • Graczyk, A. and Leśniak, W. (2014). S100A6 expression in keratinocytes and its impact on epidermal differentiation. Int. J. Biochem. Cell. Biol. 57, 135–141.CrossrefPubMedGoogle Scholar

  • Gross, S.R., Sin, C.G., Barraclough, R., and Rudland, P.S. (2014). Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell. Mol. Life Sci. 71, 1551–1579.CrossrefPubMedGoogle Scholar

  • Halawi, A., Abbas, O., and Mahalingam, M. (2014). S100 proteins and the skin: a review. J. Eur. Acad. Dermatol. Venereol. 28, 405–414.CrossrefPubMedGoogle Scholar

  • Harris, M.A, Yang. H., Low, B.E., Mukherjee, J., Guha, A., Bronson, R.T., Shultz, L.D., Israel, M.A., and Yun, K. (2008). Cancer stem cells are enriched in the side population cells in a mouse model of glioma. Cancer Res. 68, 10051–10059.CrossrefGoogle Scholar

  • Imbalzano, E., Mandraffino, G., Casciaro, M., Quartuccio, S., Saitta, A., and Gangemi, S. (2016). Pathophysiological mechanism and therapeutic role of S100 proteins in cardiac failure: a systematic review. Heart Fail. Rev. 21, 463–473.PubMedCrossrefGoogle Scholar

  • Ismail, M.F., El Boghdady, N.A, Shabayek, M.I., Awida, H.A., and Abozeed, H. (2016). Evaluation and screening of mRNA S100A genes as serological biomarkers in different stages of bladder cancer in Egypt. Tumour Biol. 37, 4621–4631.CrossrefPubMedGoogle Scholar

  • Ito, M. and Kizawa, K. (2001). Expression of calcium-binding S100 proteins A4 and A6 in regions of the epithelial sac associated with the onset of hair follicle regeneration. J. Invest. Dermatol. 116, 956–963.CrossrefPubMedGoogle Scholar

  • Jeong, J.A., Hong, S.H., Gang, E.J., Ahn, C., Hwang, S.H., Yang, I.H, Han, H., and Kim H. (2005). Differential gene expression profiling of human umbilical cord blood-derived mesenchymal stem cells by DNA microarray. Stem Cells 23, 584–593.CrossrefPubMedGoogle Scholar

  • Ji, Y.F., Hunag, H., Jiang, F., Ni, R.Z., and Xiao, M.B. (2014). S100 family signaling network and related proteins in pancreatic cancer. Int. J. Mol. Med. 33, 769–776.PubMedCrossrefGoogle Scholar

  • Joo, J.H., Kim, J.W., Lee, Y, Yoon, S.Y., Kim, J.H., Paik, S.G., and Choe, I.S. (2003). Involvement of NF-κB in the regulation of S100A6 gene expression in human hepatoblastoma cell line HepG2. Biochem. Biophys. Res. Commun. 307, 274–280.PubMedCrossrefGoogle Scholar

  • Jurewicz, E., Kasacka, I., Bankowski, E., and Filipek, A. (2014a). S100A6 and its extracellular targets in Wharton’s jelly of healthy and preeclamptic patients. Placenta 35, 386–391.CrossrefGoogle Scholar

  • Jurewicz, E., Góral, A., and Filipek, A. (2014b). S100A6 is secreted from Wharton’s jelly mesenchymal stem cells and interacts with integrin β1. Int. J. Biochem. Cell Biol. 55, 298–303.CrossrefGoogle Scholar

  • Kanojia, D., Zhou, W., Zhang, J., Jie, C., Lo, P.K., Wang, Q., and Chen, H. (2012). Proteomic profiling of cancer stem cells derived from primary tumors of HER2/Neu transgenic mice. Proteomics 12, 3407–3415.CrossrefPubMedGoogle Scholar

  • Kilańczyk, E., Filipek, S., Jastrzebska, B., and Filipek, A. (2009) CacyBP/SIP binds ERK1/2 and affects transcriptional activity of Elk-1. Biochem. Biophys. Res. Commun. 380, 54–59.CrossrefPubMedGoogle Scholar

  • Kilańczyk, E., Graczyk, A., Ostrowska, H., Kasacka, I., Leśniak, W., and Filipek A. (2012). S100A6 is transcriptionally regulated by β-catenin and interacts with a novel target, lamin A/C, in colorectal cancer cells. Cell Calcium 51, 470–477.CrossrefPubMedGoogle Scholar

  • Klein, L.L., Freitag, B.C., Gibbs, R.S., Reddy, A.P., Nagalla, S.R., and Gravett, M.G. (2005). Detection of intra-amniotic infection in a rabbit model by proteomics-based amniotic fluid analysis. Am. J. Obst. Gynecol. 193, 1302–1306.CrossrefGoogle Scholar

  • Kuźnicki, J. and Filipek, A. (1987). Purification and properties of a novel Ca2+-binding protein (10.5 kDa) from Ehrlich-ascites-tumour cells. Biochem. J. 247, 663–667.PubMedCrossrefGoogle Scholar

  • Kuźnicki, J., Kordowska, J., Puzianowska, M., and Woźniewicz, B.M. (1992). Calcyclin as a marker of human epithelial cells and fibroblasts. Exp. Cell Res. 200, 425–430.CrossrefPubMedGoogle Scholar

  • Landi, C., Bargagli, E., Bianchi, L., Gagliardi, A, Carleo, A., Bennett, D., Perari, M.G., Armini, A., Prasse, A., Rottoli, P., et al. (2013). Towards a functional proteomics approach to the comprehension of idiopathic pulmonary fibrosis, sarcoidosis, systemic sclerosis and pulmonary Langerhans cell histiocytosis. J. Proteomics 83, 60–75.PubMedCrossrefGoogle Scholar

  • Leclerc, E. and Vetter, S.W. (2015). The role of S100 proteins and their receptor RAGE in pancreatic cancer. Biochim. Biophys. Acta 1852, 2706–2711.CrossrefPubMedGoogle Scholar

  • Leclerc, E., Fritz, G., Vetter, S.W., and Heizmann, C.W. (2009). Binding of S100 proteins to RAGE: an update. Biochim. Biophys. Acta 1793, 993–1007.PubMedCrossrefGoogle Scholar

  • Lee, Y.S., Chen, P.W., Tsai, P.J., Su, S.H., and Liao, P.C. (2006). Proteomics analysis revealed changes in rat bronchoalveolar lavage fluid proteins associated with oil mist exposure. Proteomics 6, 2236–2250.CrossrefPubMedGoogle Scholar

  • Lerchenmüller, C., Heißenberg, J., Damilano, F., Bezzeridis, V.J., Krämer, I., Bochaton-Piallat, M.L., Hirschberg, K., Busch, M., Katus, H.A., Peppel, K., et al. (2016). S100A6 regulates endothelial cell cycle progression by attenuating antiproliferative signal transducers and activators of transcription 1 signaling. Arterioscler. Thromb. Vasc. Biol. 36, 1854–1867.PubMedCrossrefGoogle Scholar

  • Leśniak, W. and Filipek, A. (1996). Ca2+-dependent interaction of calcyclin with membrane. Biochem. Biophys. Res. Commun. 220, 269–273.PubMedCrossrefGoogle Scholar

  • Leśniak, W. and Graczyk-Jarzynka, A. (2015). The S100 proteins in epidermis: topology and function. Biochim. Biophys. Acta 1850, 2563–2572.PubMedCrossrefGoogle Scholar

  • Leśniak, W., Jezierska, A., and Kuźnicki, J. (2000). Upstream stimulatory factor is involved in the regulation of the human calcyclin (S100A6) gene. Biochim. Biophys. Acta 1517, 73–81.CrossrefPubMedGoogle Scholar

  • Leśniak, W., Słomnicki, Ł.P., and Kuźnicki, J. (2007). Epigenetic control of the S100A6 (calcyclin) gene expression. J. Invest. Dermatol 127, 2307–2314.CrossrefPubMedGoogle Scholar

  • Leśniak, W., Słomnicki, Ł.P., and Filipek, A. (2009). S100A6 – new facts and features. Biochem. Biophys. Res. Commun. 390, 1087–1092.CrossrefPubMedGoogle Scholar

  • Li, Z., Tang, M., Ling, B., Liu, S., Zheng, Y., Nie, C., Yuan, Z., Zhou, L., Guo, G., Tong, A., et al. (2014). Increased expression of S100A6 promotes cell proliferation and migration in human hepatocellular carcinoma. J. Mol. Med. (Berl) 92, 291–303.CrossrefPubMedGoogle Scholar

  • Li, Y., Wagner, E.R., Yan, Z., Wang, Z., Luther, G., Jiang, W., Ye, J., Wei, Q., Wang, J., Zhao, L., et al. (2015). The calcium-binding protein S100A6 accelerates human osteosarcoma growth by promoting cell proliferation and inhibiting osteogenic differentiation. Cell. Physiol. Biochem. 37, 2375–2392.CrossrefPubMedGoogle Scholar

  • Li, A, Shi, D., Xu, B., Wang, J., Tang, Y.L., Xiao, W., Shen, G., Deng, W., and Zhao, C. (2017). S100A6 promotes cell proliferation in human nasopharyngeal carcinoma via the p38/MAPK signaling pathway. Mol. Carcinog. 56, 972–984.PubMedCrossrefGoogle Scholar

  • Liu, Z., Zhang, X., Chen, M., Cao, Q., and Huang, D. (2015). Effect of S100A6 over-expression on β-catenin in endometriosis. J. Obstet. Gynaecol. Res. 41, 1457–1462.CrossrefPubMedGoogle Scholar

  • Ludvigsen, M., Jacobsen, C., Maunsbach, A.B., and Honoré, B. (2009). Identification and characterization of novel ERC-55 interacting proteins: evidence for the existence of several ERC-55 splicing variants; including the cytosolic ERC-55-C. Proteomics 9, 5267–5287.CrossrefPubMedGoogle Scholar

  • Maletzki, C., Bodammer, P., Breitrück, A., and Kerkhoff C. (2012). S100 proteins as diagnostic and prognostic markers in colorectal and hepatocellular carcinoma. Hepat. Mon. 12, e7240.PubMedGoogle Scholar

  • Mignone, J.L., Roig-Lopez, J.L, Fedtsova, N., Schones, D.E., Manganas, L.N., Maletic-Savatic, M., Keyes, W.M., Mills, A.A., Gleiberman, A., Zhang, M.Q., et al. (2007). Neural potential of a stem cell population in the hair follicle. Cell Cycle 6, 2161–2170.PubMedCrossrefGoogle Scholar

  • Moravkova, P., Kohoutova, D., Rejchrt, S., Cyrany, J., and Bures, J. (2016). Role of S100 proteins in colorectal, carcinogenesis. Gastroenterol. Res. Pract. 2016, 2632703.PubMedGoogle Scholar

  • Moroz, O.V., Wilson, K.S., and Bronstein, I.B. (2011). The role of zinc in the S100 proteins: insights from the X-ray structures. Amino Acids 41, 761–772.CrossrefPubMedGoogle Scholar

  • Nishi, M., Matsumoto, K., Kobayashi, M., Yanagita, K., Matsumoto, T., Nagashio, R., Ishii, D., Fujita, T., Sato, Y., and Iwamura, M. (2014). Serum expression of S100A6 is a potential detection marker in patients with urothelial carcinoma in the urinary bladder. Biomed. Res. 35, 351–356.PubMedCrossrefGoogle Scholar

  • Ouji, Y., Yoshikawa, M., Nishiofuku, M., Ouji-Sageshima, N., Kubo, A., and Ishizaka, S. (2010). Effects of Wnt-10b on proliferation and differentiation of adult murine skin-derived CD34 and CD49f double-positive cells. J. Biosci. Bioeng. 110, 2217–2122.Google Scholar

  • Patgaonkar, M., Aranha, C., Bhonde, G., and Reddy, K.V. (2011). Identification and characterization of anti-microbial peptides from rabbit vaginal fluid. Vet. Immunol. Immunopathol. 139, 176–186.CrossrefPubMedGoogle Scholar

  • Persson, A.I., Petritsch, C., Swartling, F.J., Itsara, M., Sim, F.J., Auvergne, R., Goldenberg, D.D., Vandenberg, S.R., Nguyen, K.N., Yakovenko, S., et al. (2010). Non-stem cell origin for oligodendroglioma. Cancer Cell 18, 669–682.CrossrefPubMedGoogle Scholar

  • Rehman, I., Cross, S.S., Catto, J.W., Leiblich, A., Mukherjee, A., Azzouzi, A.R., Leung, H.Y., and Hamdy, F.C. (2005). Promoter hyper-methylation of calcium binding proteins S100A6 and S100A2 in human prostate cancer. Prostate 65, 322–330.PubMedCrossrefGoogle Scholar

  • Rijsewijk, F., Schuermann, M., Wagenaar, E., Parren, P., Weigel, D., and Nusse, R. (1987). The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50, 649–657.CrossrefPubMedGoogle Scholar

  • Sastry, M., Ketchem, R.R., Crescenzi, O., Weber, C., Lubienski, M.J., Hidaka, H., and Chazin, W.J. (1998). The three-dimensional structure of Ca2+-bound calcyclin: implications for Ca2+-signal transduction by S100 proteins. Structure 6, 223–231.CrossrefGoogle Scholar

  • Sbroggiò, M., Ferretti, R., Percivalle, E., Gutkowska, M., Zylicz, A., Michowski, W., Kuznick,i J., Accornero, F., Pacchioni, B., Lanfranchi, G., et al. (2008) The mammalian CHORD-containing protein melusin is a stress response protein interacting with Hsp90 and Sgt1. FEBS Lett. 582, 1788–1794.PubMedCrossrefGoogle Scholar

  • Shimamoto, S., Takata, M., Tokuda, M., Oohira, F., Tokumitsu, H., and Kobayashi, R. (2008) Interactions of S100A2 and S100A6 with the tetratricopeptide repeat proteins, Hsp90/Hsp70-organizing protein and kinesin light chain. J. Biol. Chem. 283, 28246–28258.CrossrefPubMedGoogle Scholar

  • Shimamoto, S., Kubota, Y., Tokumitsu, H., and Kobayashi, R. (2010). S100 proteins regulate the interaction of Hsp90 with cyclophilin 40 and FKBP52 through their tetratricopeptide repeats. FEBS Lett. 584, 1119–1125.CrossrefPubMedGoogle Scholar

  • Shimamoto, S., Tsuchiya, M., Yamaguchi, F., Kubota, Y., Tokumitsu, H., and Kobayashi, R. (2014). Ca2+/S100 proteins inhibit the interaction of FKBP38 with Bcl-2 and Hsp90. Biochem. J. 458, 141–152.PubMedCrossrefGoogle Scholar

  • Słomnicki, Ł.P., Nawrot, B., and Leśniak, W. (2009) S100A6 binds p53 and affects its activity. Int. J. Biochem. Cell Biol. 41, 784–790.CrossrefPubMedGoogle Scholar

  • Spiechowicz, M., Zylicz, A., Bieganowski, P., Kuznicki, J., and Filipek, A. (2007). Hsp70 is a new target of Sgt1 – an interaction modulated by S100A6. Biochem. Biophys. Res. Commun. 357, 1148–1153.PubMedCrossrefGoogle Scholar

  • Stradal, T.B. and Gimona, M. (1999). Ca2+-dependent association of S100A6 (Calcyclin) with the plasma membrane and the nuclear envelope. J. Biol. Chem. 274, 31593–31596.CrossrefGoogle Scholar

  • Takata, M., Shimamoto, S., Yamaguchi, F., Tokuda, M., Tokumitsu, H., and Kobayashi, R. (2010). Regulation of nuclear localization signal-importin α interaction by Ca2+/S100A6. FEBS Lett. 584, 4517–4523.CrossrefPubMedGoogle Scholar

  • Taylor, G., Lehrer, M.S., Jensen, P.J., Sun, T.T., and Lavker, R.M. (2000). Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102, 451–461.PubMedCrossrefGoogle Scholar

  • van Dieck, J., Brandt, T., Teufel, D.P., Veprintsev, D.B., Joerger, A.C., and Fersht, A.R. (2010a). Molecular basis of S100 proteins interacting with the p53 homologs p63 and p73. Oncogene 29, 2024–2035.CrossrefGoogle Scholar

  • van Dieck, J., Lum, J.K., Teufel, D.P., and Fersht, A.R. (2010b). S100 proteins interact with the N-terminal domain of MDM2. FEBS Lett. 584, 3269–3274.CrossrefGoogle Scholar

  • Wang, T., Liang, Y., Thakur, A., Zhang, S., Yang, T., Chen, T., Gao, L., Chen, M., and Ren, H. (2016). Diagnostic significance of S100A2 and S100A6 levels in sera of patients with non-small cell lung cancer. Tumour Biol. 37, 2299–2304.PubMedCrossrefGoogle Scholar

  • Wasik, U., Kadziolka, B., Kilanczyk, E., and Filipek, A. (2016) Influence of S100A6 on CacyBP/SIP phosphorylation and Elk-1 transcriptional activity in neuroblastoma NB2a cells. J. Cell Biochem. 117, 126–131.PubMedCrossrefGoogle Scholar

  • Wei, B.R., Hoover, S,B,, Ross, M.M., Zhou, W., Meani, F., Edwards, J.B., Spehalski, E.I., Risinger, J.I., Alvord, W.G., Quiñones, O.A., et al. (2009). Serum S100A6 concentration predicts peritoneal tumor burden in mice with epithelial ovarian cancer and is associated with advanced stage in patients. PLoS One 4, e7670.PubMedCrossrefGoogle Scholar

  • Willis, N.D., Cox, T.R., Rahman-Casans, S.F., Smith, K., Przyborski, S.A., van den Brandt, P., van Engeland, M., Weijenberg, M., Wilson, R.G., de Bruine, A., et al. (2008). Lamin A/C is a risk biomarker in colorectal cancer. PLoS One 3, e2988.CrossrefPubMedGoogle Scholar

  • Yamada, J. and Jinno, S. (2014). S100A6 (calcyclin) is a novel marker of neural stem cells and astrocyte precursors in the subgranular zone of the adult mouse hippocampus. Hippocampus 24, 89–101.CrossrefPubMedGoogle Scholar

  • Yamaguchi, F., Umeda, Y., Shimamoto, S., Tsuchiya, M., Tokumitsu, H., Tokuda, M., and Kobayashi, R. (2012). S100 proteins modulate protein phosphatase 5 function: a link between Ca2+ signal transduction and protein dephosphorylation. J. Biol. Chem. 287, 13787–13798.CrossrefPubMedGoogle Scholar

  • Yamaguchi, F., Yamamura, S., Shimamoto, S., Tokumitsu, H., Tokuda, M., and Kobayashi, R. (2014). Suramin is a novel activator of PP5 and biphasically modulates S100-activated PP5 activity. Appl. Biochem. Biotechnol. J172, 237–247.CrossrefGoogle Scholar

  • Yammani, R.R. (2012). S100 proteins in cartilage: role in arthritis. Biochim. Biophys. Acta 1822, 600–606.CrossrefPubMedGoogle Scholar

  • Yang, Q., O’Hanlon, D., Heizmann, C.W., and Marks, A. (1999). Demonstration of heterodimer formation between S100B and S100A6 in the yeast two-hybrid system and human melanoma. Exp. Cell Res. 246, 501–509.CrossrefPubMedGoogle Scholar

  • Yatime, L., Betzer, C., Jensen, R.K., Mortensen, S., Jensen, P.H., and Andersen, G.R. (2016). The structure of the RAGE:S100A6 complex reveals a unique mode of homodimerization for S100 proteins. Structure 24, 2043–2052.PubMedCrossrefGoogle Scholar

  • Zackular, J.P., Chazin, W.J., and Skaar, E.P. (2015). Nutritional immunity: S100 proteins at the host-pathogen interface. J. Biol. Chem. 290, 18991–18998.PubMedCrossrefGoogle Scholar

  • Zhang, S.P., Wu, Z.Z., Wu, Y.W., Su, S.B., and Tong J. (2010). [Mechanism study of adaptive response in high background radiation area of Yangjiang in China]. Zhonghua Yu Fang Yi Xue Za Zhi 44, 815–819.Google Scholar

  • Zhang, J., Zhang, K., Jiang, X., and Zhang, J. (2014). S100A6 as a potential serum prognostic biomarker and therapeutic target in gastric cancer. Digest. Dis. Sci. 59, 2136–2144.CrossrefGoogle Scholar

About the article

Received: 2017-03-03

Accepted: 2017-03-21

Published Online: 2017-03-25

Published in Print: 2017-09-26


Citation Information: Biological Chemistry, Volume 398, Issue 10, Pages 1087–1094, ISSN (Online) 1437-4315, ISSN (Print) 1431-6730, DOI: https://doi.org/10.1515/hsz-2017-0125.

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