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Gastroenterology Research and Practice
Volume 2016, Article ID 2632703, 7 pages
http://dx.doi.org/10.1155/2016/2632703
Review Article

Role of S100 Proteins in Colorectal Carcinogenesis

12nd Department of Internal Medicine-Gastroenterology, Charles University in Praha, Faculty of Medicine at Hradec Kralove, University Teaching Hospital, Sokolska 581, 500 05 Hradec Kralove, Czech Republic
2Division of Surgery and Interventional Science, University College London, 67-73 Riding House Street, London W1W 7EJ, UK

Received 20 August 2015; Revised 22 November 2015; Accepted 29 November 2015

Academic Editor: Bisweswar Nandi

Copyright © 2016 Paula Moravkova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. C. Deloulme, G. O. Mbele, and J. Baudier, “S100 proteins. From purification to functions,” Methods in Molecular Biology, vol. 172, pp. 185–198, 2002. View at Google Scholar · View at Scopus
  2. R. Donato, B. R. Cannon, G. Sorci et al., “Functions of S100 proteins,” Current Molecular Medicine, vol. 13, no. 1, pp. 24–57, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. B. W. Moore and D. McGregor, “Chromatographic and electrophoretic fractionation of soluble proteins of brain and liver,” The Journal of Biological Chemistry, vol. 240, pp. 1647–1653, 1965. View at Google Scholar · View at Scopus
  4. A. L. Rubin and K. H. Stenzel, “In vitro synthesis of brain protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 53, no. 5, pp. 963–968, 1965. View at Google Scholar
  5. R. H. Kretsinger and C. E. Nockolds, “Carp muscle calcium-binding protein. II. Structure determination and general description,” The Journal of Biological Chemistry, vol. 248, no. 9, pp. 3313–3326, 1973. View at Google Scholar · View at Scopus
  6. F. Suzuki, T. Nakajima, and K. Kato, “Peripheral distribution of nervous-system specific S100 protein in rat,” Journal of Biochemistry, vol. 92, no. 3, pp. 835–838, 1982. View at Google Scholar · View at Scopus
  7. H. Kawasaki, S. Nakayama, and R. H. Kretsinger, “Classification and evolution of EF-hand proteins,” Biometals, vol. 11, no. 4, pp. 277–295, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Weinman, “Calcium-binding proteins: an overview,” Journal de Biologie Buccale, vol. 19, no. 1, pp. 90–98, 1991. View at Google Scholar · View at Scopus
  9. L. Santamaria-Kisiel, A. C. Rintala-Dempsey, and G. S. Shaw, “Calcium-dependent and -independent interactions of the S100 protein family,” Biochemical Journal, vol. 396, no. 2, pp. 201–214, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Denessiouk, S. Permyakov, A. Denesyuk, E. Permyakov, and M. S. Johnson, “Two structural motifs within canonical EF-hand calcium-binding domains identify five different classes of calcium buffers and sensors,” PLoS ONE, vol. 9, no. 10, Article ID e109287, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. A. M. Kraemer, L. R. Saraiva, and S. I. Korsching, “Structural and functional diversification in the teleost S100 family of calcium-binding proteins,” BMC Evolutionary Biology, vol. 8, no. 1, article 48, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. International Agency for Research on Cancer, GLOBOCAN 2012: Estimated Cancer Incidence, Mortality and Prevalence Worldwide in 2012, IARC, Lyon, France, 2013.
  15. H. Chen, C. Xu, Q. Jin, and Z. Liu, “S100 protein family in human cancer,” American Journal of Cancer Research, vol. 4, no. 2, pp. 89–115, 2014. View at Google Scholar
  16. S. Ghavami, C. Kerkhoff, W. J. Chazin et al., “S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1783, no. 2, pp. 297–311, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. I. P. Korndörfer, F. Brueckner, and A. Skerra, “The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting α-helices can determine specific association of two EF-hand proteins,” Journal of Molecular Biology, vol. 370, no. 5, pp. 887–898, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. T. E. Kehl-Fie, S. Chitayat, M. I. Hood et al., “Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus,” Cell Host and Microbe, vol. 10, no. 2, pp. 158–164, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Ryckman, K. Vandal, P. Rouleau, M. Talbot, and P. A. Tessier, “Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion,” The Journal of Immunology, vol. 170, no. 6, pp. 3233–3242, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Vogl, K. Tenbrock, S. Ludwig et al., “Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock,” Nature Medicine, vol. 13, no. 9, pp. 1042–1049, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Sinha, C. Okoro, D. Foell, H. H. Freeze, S. Ostrand-Rosenberg, and G. Srikrishna, “Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells,” The Journal of Immunology, vol. 181, no. 7, pp. 4666–4675, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Hiratsuka, A. Watanabe, H. Aburatani, and Y. Maru, “Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis,” Nature Cell Biology, vol. 8, no. 12, pp. 1369–1375, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Saha, Y.-C. Lee, Z. Zhang, G. Chandra, S.-B. Su, and A. B. Mukherjee, “Lack of an endogenous anti-inflammatory protein in mice enhances colonization of B16F10 melanoma cells in the lungs,” The Journal of Biological Chemistry, vol. 285, no. 14, pp. 10822–10831, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Ghavami, C. Kerkhoff, M. Los, M. Hashemi, C. Sorg, and F. Karami-Tehrani, “Mechanism of apoptosis induced by S100A8/A9 in colon cancer cell lines: the role of ROS and the effect of metal ions,” Journal of Leukocyte Biology, vol. 76, no. 1, pp. 169–175, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Ghavami, I. Rashedi, B. M. Dattilo et al., “S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway,” Journal of Leukocyte Biology, vol. 83, no. 6, pp. 1484–1492, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Ichikawa, R. Williams, L. Wang, T. Vogl, and G. Srikrishna, “S100A8/A9 activate key genes and pathways in colon tumor progression,” Molecular Cancer Research, vol. 9, no. 2, pp. 133–148, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. O. Turovskaya, D. Foell, P. Sinha et al., “RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis,” Carcinogenesis, vol. 29, no. 10, pp. 2035–2043, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. F. S. Lehmann, F. Trapani, I. Fueglistaler et al., “Clinical and histopathological correlations of fecal calprotectin release in colorectal carcinoma,” World Journal of Gastroenterology, vol. 20, no. 17, pp. 4994–4999, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Schmidt-Hansen, D. Örnås, M. Grigorian et al., “Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity,” Oncogene, vol. 23, no. 32, pp. 5487–5495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Ebralidze, E. Tulchinsky, M. Grigorian et al., “Isolation and characterization of a gene specifically expressed in different metastatic cells and whose deduced gene product has a high degree of homology to a Ca2+-binding protein family,” Genes & development, vol. 3, no. 7, pp. 1086–1093, 1989. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Liu, W. Tang, J. Wang et al., “Clinicopathological and prognostic significance of S100A4 overexpression in colorectal cancer: a meta-analysis,” Diagnostic Pathology, vol. 8, article 181, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Boye, J. M. Nesland, B. Sandstad, G. M. Mælandsmo, and K. Flatmark, “Nuclear S100A4 is a novel prognostic marker in colorectal cancer,” European Journal of Cancer, vol. 46, no. 16, pp. 2919–2925, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. U. Sack and U. Stein, “Wnt up your mind—intervention strategies for S100A4-induced metastasis in colon cancer,” General Physiology and Biophysics, vol. 28, pp. F55–F64, 2009. View at Google Scholar · View at Scopus
  34. M. Kriajevska, M. Fischer-Larsen, E. Moertz et al., “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),” The Journal of Biological Chemistry, vol. 277, no. 7, pp. 5229–5235, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Grigorian, S. Andresen, E. Tulchinsky et al., “Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction,” The Journal of Biological Chemistry, vol. 276, no. 25, pp. 22699–22708, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Semov, M. J. Moreno, A. Onichtchenko et al., “Metastasis-associated protein S100A4 induces angiogenesis through interaction with annexin II and accelerated plasmin formation,” The Journal of Biological Chemistry, vol. 280, no. 21, pp. 20833–20841, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. B. Rubinfeld, I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis, “Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly,” Science, vol. 272, no. 5264, pp. 1023–1026, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Mann, M. Gelos, A. Siedow et al., “Target genes of β-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 4, pp. 1603–1608, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. U. Sack, W. Walther, D. Scudiero et al., “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, vol. 22, no. 18, pp. 3344–3354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. U. Stein, F. Arlt, J. Smith et al., “Intervening in β-catenin signaling by sulindac inhibits S100A4-dependent colon cancer metastasis,” Neoplasia, vol. 13, no. 2, pp. 131–144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Komatsu, A. Andoh, S. Ishiguro et al., “Increased expression of S100A6 (calcyclin), a calcium-binding protein of the S100 family, in human colorectal adenocarcinomas,” Clinical Cancer Research, vol. 6, no. 1, pp. 172–177, 2000. View at Google Scholar · View at Scopus
  42. E. Kilańczyk, A. Graczyk, H. Ostrowska, I. Kasacka, W. Leśniak, and A. Filipek, “S100A6 is transcriptionally regulated by β-catenin and interacts with a novel target, lamin A/C, in colorectal cancer cells,” Cell Calcium, vol. 51, no. 6, pp. 470–477, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Melle, G. Ernst, B. Schimmel et al., “Different expression of calgizzarin (S100A11) in normal colonic epithelium, adenoma and colorectal carcinoma,” International Journal of Oncology, vol. 28, no. 1, pp. 195–200, 2006. View at Google Scholar · View at Scopus
  44. M.-Y. Huang, H.-M. Wang, T.-S. Tok et al., “EVI2B, ATP2A2, S100B, TM4SF3, and OLFM4 as potential prognostic markers for postoperative Taiwanese colorectal cancer patients,” DNA and Cell Biology, vol. 31, no. 4, pp. 625–635, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Becker, V. Gerke, E. Kube, and K. Weber, “S100P, a novel Ca2+-binding protein from human placenta. cDNA cloning, recombinant protein expression and Ca2+ binding properties,” European Journal of Biochemistry, vol. 207, no. 2, pp. 541–547, 1992. View at Publisher · View at Google Scholar · View at Scopus
  46. F. F. Lam, L. Jankova, O. F. Dent et al., “Identification of distinctive protein expression patterns in colorectal adenoma,” Proteomics Clinical Applications, vol. 4, no. 1, pp. 60–70, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Chandramouli, M. E. Mercado-Pimentel, A. Hutchinson et al., “The induction of S100p expression by the Prostaglandin E2 (PGE2)/EP4 receptor signaling pathway in colon cancer cells,” Cancer Biology & Therapy, vol. 10, no. 10, pp. 1056–1066, 2014. View at Publisher · View at Google Scholar
  48. L. Y. Cao, Y. Yin, H. Li, Y. Jiang, and H. F. Zhang, “Expression and clinical significance of S100A2 and p63 in esophageal carcinoma,” World Journal of Gastroenterology, vol. 15, no. 33, pp. 4183–4188, 2009. View at Google Scholar
  49. O.-J. Lee, S.-M. Hong, M. H. Razvi et al., “Expression of calcium-binding proteins S100A2 and S100A4 in Barrett's adenocarcinomas,” Neoplasia, vol. 8, no. 10, pp. 843–850, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. A. H. Zaidi, V. Gopalakrishnan, P. M. Kasi et al., “Evaluation of a 4-protein serum biomarker panel-biglycan, annexin-A6, myeloperoxidase, and protein S100-A9 (B-AMP)-for the detection of esophageal adenocarcinoma,” Cancer, vol. 120, no. 24, pp. 3902–3913, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. Y.-F. Liu, Q.-Q. Liu, X. Wang, and C.-H. Luo, “Clinical significance of S100A2 expression in gastric cancer,” Tumor Biology, vol. 35, no. 4, pp. 3731–3741, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. Q. Zhang, M. Zhu, W. Cheng et al., “Downregulation of 425G>A variant of calcium-binding protein S100A14 associated with poor differentiation and prognosis in gastric cancer,” Journal of Cancer Research and Clinical Oncology, vol. 141, no. 4, pp. 691–703, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. Z. Ling and R. Li, “Clinicopathological and prognostic value of S100A4 expression in gastric cancer: a meta-analysis,” International Journal of Biological Markers, vol. 29, no. 2, pp. e99–e111, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Wang, L.-B. Zhou, and X.-H. Li, “S100A4 expression and prognosis of gastric cancer: a meta-analysis,” Genetics and Molecular Research, vol. 13, no. 4, pp. 10398–10403, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Zhang, K. Zhang, X. Jiang, and J. Zhang, “S100A6 as a potential serum prognostic biomarker and therapeutic target in gastric cancer,” Digestive Diseases and Sciences, vol. 59, no. 9, pp. 2136–2144, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Liu, X. Li, G. L. Dong et al., “In silico analysis and verification of S100 gene expression in gastric cancer,” BMC Cancer, vol. 8, no. 1, article 261, 2008. View at Publisher · View at Google Scholar
  57. L. Wang, E. W. Y. Chang, S. Wong, S.-M. Ong, D. Q. Y. Chong, and K. L. Ling, “Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma S100A8/A9 proinflammatory proteins,” Journal of Immunology, vol. 190, no. 2, pp. 794–804, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. J.-B. Bachet, R. Maréchal, P. Demetter et al., “S100A2 is a predictive biomarker of adjuvant therapy benefit in pancreatic adenocarcinoma,” European Journal of Cancer, vol. 49, no. 12, pp. 2643–2653, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. Y.-F. Ji, H. Huang, F. Jiang, R.-Z. Ni, and M.-B. Xiao, “S100 family signaling network and related proteins in pancreatic cancer (review),” International Journal of Molecular Medicine, vol. 33, no. 4, pp. 769–776, 2014. View at Publisher · View at Google Scholar
  60. K. Ohuchida, K. Mizumoto, S. Ohhashi et al., “S100A11, a putative tumor suppressor gene, is overexpressed in pancreatic carcinogenesis,” Clinical Cancer Research, vol. 12, no. 18, pp. 5417–5422, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Kuźnicki and A. Filipek, “Purification and properties of a novel Ca2+-binding protein (10.5 kDa) from Ehrlich-ascites-tumour cells,” Biochemical Journal, vol. 247, no. 3, pp. 663–667, 1987. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Stulík, J. Österreicher, K. Koupilová et al., “Differential expression of the Ca2+ binding S100A6 protein in normal, preneoplastic and neoplastic colon mucosa,” European Journal of Cancer, vol. 36, no. 8, pp. 1050–1059, 2000. View at Publisher · View at Google Scholar · View at Scopus
  63. E. Leclerc, G. Fritz, M. Weibel, C. W. Heizmann, and A. Galichet, “S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31317–31331, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Duan, R. Wu, Z. Zou et al., “S100A6 stimulates proliferation and migration of colorectal carcinoma cells through activation of the MAPK pathways,” International Journal of Oncology, vol. 44, no. 3, pp. 781–790, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Melle, G. Ernst, B. Schimmel, A. Bleul, and F. von Eggeling, “Colon-derived liver metastasis, colorectal carcinoma, and hepatocellular carcinoma can be discriminated by the Ca2+-binding proteins S100A6 and S100A11,” PLoS ONE, vol. 3, no. 12, Article ID e3767, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. H. He, J. Li, S. Weng, M. Li, and Y. Yu, “S100A11: diverse function and pathology corresponding to different target proteins,” Cell Biochemistry and Biophysics, vol. 55, no. 3, pp. 117–126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Sakaguchi, M. Miyazaki, Y. Inoue et al., “Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts,” Journal of Cell Biology, vol. 149, no. 6, pp. 1193–1206, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. D. L. Cecil, K. Johnson, J. Rediske, M. Lotz, A. M. Schmidt, and R. Terkeltaub, “Inflammation-induced chondrocyte hypertrophy is driven by receptor for advanced glycation end products,” Journal of Immunology, vol. 175, no. 12, pp. 8296–8302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Stulík, K. Koupilová, J. Österreicher et al., “Protein abundance alterations in matched sets of macroscopically normal colon mucosa and colorectal carcinoma,” Electrophoresis, vol. 20, no. 18, pp. 3638–3646, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. M.-Y. Huang, H.-M. Wang, H.-J. Chang, C.-P. Hsiao, J.-Y. Wang, and S.-R. Lin, “Overexpression of s100b, tm4sf4, and olfm4 genes is correlated with liver metastasis in taiwanese colorectal cancer patients,” DNA and Cell Biology, vol. 31, no. 1, pp. 43–49, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Emoto, R. Kobayashi, H. Akatsuka, and H. Hidaka, “Purification and characterization of a new member of the S-100 protein family from human placenta,” Biochemical and Biophysical Research Communications, vol. 182, no. 3, pp. 1246–1253, 1992. View at Publisher · View at Google Scholar · View at Scopus
  72. S. E. Dowen, T. Crnogorac-Jurcevic, R. Gangeswaran et al., “Expression of S100P and its novel binding partner S100PBPR in early pancreatic cancer,” The American Journal of Pathology, vol. 166, no. 1, pp. 81–92, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Dong, F. Wang, X. Yin et al., “Overexpression of S100P promotes colorectal cancer metastasis and decreases chemosensitivity to 5-FU in vitro,” Molecular and Cellular Biochemistry, vol. 389, no. 1-2, pp. 257–264, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. Q. Wang, Y.-N. Zhang, G.-L. Lin et al., “S100P, a potential novel prognostic marker in colorectal cancer,” Oncology Reports, vol. 28, no. 1, pp. 303–310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Shen, A. Sundstedt, M. Ciesielski et al., “Tasquinimod modulates suppressive myeloid cells and enhances cancer immunotherapies in murine models,” Cancer Immunology Research, vol. 3, no. 2, pp. 136–148, 2015. View at Publisher · View at Google Scholar
  76. E. Raymond, A. Dalgleish, J.-E. Damber, M. Smith, and R. Pili, “Mechanisms of action of tasquinimod on the tumour microenvironment,” Cancer Chemotherapy and Pharmacology, vol. 73, no. 1, pp. 1–8, 2014. View at Publisher · View at Google Scholar · View at Scopus