S100 family signaling network and related proteins in pancreatic cancer (review)

International Journal of Molecular Medicine

Volumn 33, Issue 4, 2014, Pages 769-776

  Ji, Yi Fei ^a   Huang, Hua ^a   Jiang, Feng ^a   Ni, Run Zhou ^a   Xiao, Ming Bing ^a  

^a NANTONG UNIVERSITY   (China)

Author keywords

Biomarkers; Expression; Molecular targets; Pancreatic cancer; S100 proteins

Indexed keywords

CALVASCULIN; CYTOSKELETON PROTEIN; PROTEIN P21; PROTEIN P53; PROTEIN S 100; PROTEIN S 100A11; PROTEIN S 100A2; PROTEIN S 100A6; PROTEIN S 100P; UNCLASSIFIED DRUG;

CELL MEMBRANE; EXTRACELLULAR MATRIX; HUMAN; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; MOLECULAR TARGETED THERAPY; PANCREATIC NEOPLASMS; S100 PROTEINS; SIGNAL TRANSDUCTION;

EID: 84899503472     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2014.1633     Document Type: Review

References (90)

1. Li N, Song MM, Chen XH, Liu LH and Li FS: S100A4 siRNA inhibits human pancreatic cancer cell invasion in vitro. Biomed Environ Sci 25: 465-470, 2012.
2. Arumugam T and Logsdon CD: S100P: a novel therapeutic target for cancer. Amino acids 41: 893-899, 2011.
3. Xie L, Ni WK, Chen XD, Xiao MB, Chen BY, He S, Lu CH, Li XY, Jiang F and Ni RZ: The expressions and clinical signifi- cances of tissue and serum galectin-3 in pancreatic carcinoma. J Cancer Res Clin Oncol 138: 1035-1043, 2012.
4. Danovi SA, Wong HH and Lemoine NR: Targeted therapies for pancreatic cancer. Br Med Bull 87: 97-130, 2008.
5. Rezvanpour A and Shaw GS: Unique S100 target protein interactions. Gen Physiol Biophys 28: F39-F46, 2009.
6. Yao R, Lopez-Beltran A, Maclennan GT, Montironi R, Eble JN and Cheng L: Expression of S100 protein family members in the pathogenesis of bladder tumors. Anticancer Res 27: 3051-3058, 2007. (Pubitemid 47607526)
7. Salama I, Malone PS, Mihaimeed F and Jones JL: A review of the S100 proteins in cancer. Eur J Surg Oncol 34: 357-364, 2008. (Pubitemid 351381290)
8. 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 33: 637-668, 2001.
9. Marenholz I, Heizmann CW and Fritz G: S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322: 1111-1122, 2004. (Pubitemid 39164640)
10. Moore BW: A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19: 739-744, 1965.
11. Zimmer DB, Cornwall EH, Landar A and Song W: The S100 protein family: history, function, and expression. Brain Res Bull 37: 417-429, 1995.
12. Berge G and Mælandsmo GM: Evaluation of potential interactions between the metastasis-associated protein S100A4 and the tumor suppressor protein p53. Amino Acids 41: 863-873, 2011.
13. Komatsu K, Kobune-Fujiwara Y, Andoh A, et al: Increased expression of S100A6 at the invading fronts of the primary lesion and liver metastasis in patients with colorectal adenocarcinoma. Br J Cancer 83:769-774, 2000.
14. 2+)-binding proteins S100A6 and S100A11. PloS One 3: e3767, 2008.
15. Schäfer BW and Heizmann CW: The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21: 134-140, 1996.
16. Mishra SK, Siddique HR and Saleem M: S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence. Cancer Metastasis Rev 31: 163-172, 2012.
17. Heizmann CW, Ackermann GE and Galichet A: Pathologies involving the S100 proteins and RAGE. Subcell Biochem 45: 93-138, 2007.
18. Saleem M, Kweon MH, Johnson JJ, et al: 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, 2006. (Pubitemid 44527813)
19. Gross SR, Sin CG, Barraclough R and Rudland PS: Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell Mol Life Sci 30: June 30, 2013 (Epub ahead of print).
20. Sorci G, Riuzzi F, Giambanco I and Donato R: RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta 1833: 101-109, 2012.
21. Xie J, Méndez JD, Méndez-Valenzuela and Aguilar-Hernández MM: Cellular signalling of the receptor for advanced glycation end products (RAGE). Cell Signal 25: 2185-2197, 2013.
22. Maletzki C, Bodammer P, Breitrück A and Kerkhoff C: S100 proteins as diagnostic and prognostic markers in colorectal and hepatocellular carcinoma. Hepat Mon 12: e7240, 2012.
23. Volz HC, Laohachewin D, Seidel C, et al: S100A8/A9 aggravates post-ischemic heart failure through activation of RAGE-dependent NF-κB signaling. Basic Res Cardiol 107: 250, 2012.
24. 2+-bound human S100A11. Biomol NMR Assign 7: 211-214, 2013.
25. Arumugam T, Ramachandran V, Gomez SB, Schmidt AM and Logsdon CD: S100P-derived RAGE antagonistic peptide reduces tumor growth and metastasis. Clin Cancer Res 18: 4356-4364, 2012.
26. Arumugam T, Ramachandran V, Sun D, et al: Designing and developing S100P inhibitor 5-methyl cromolyn for pancreatic cancer therapy. Mol Cancer Ther 12: 654-662, 2013.
27. Ohuchida K, Mizumoto K, Miyasaka Y, et al: Over-expression of S100A2 in pancreatic cancer correlates with progression and poor prognosis. J Pathol 213: 275-282, 2007. (Pubitemid 350074017)
28. Leclerc E, Fritz G, Weibel M, Heizmann CW and Calichet A: S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem 282: 31317-31331, 2007. (Pubitemid 350044892)
29. 2+ signaling S100 proteins and RAGE in translational medicine. Front Biosci (Schol Ed) 3: 1232-1262, 2011.
30. Filipek A, Michowski W and Kuznicki J: Involvement of S100A6 (calcyclin) and its binding partners in intracellular signaling pathways. Adv Enzyme Regul 48: 225-239, 2008.
31. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R and Rauuala H: Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275: 40096-40105, 2000. (Pubitemid 32064635)
32. Taguchi A, Blood DC, del Toro G, et al: Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 405: 354-360, 2000. (Pubitemid 30337069)
33. Lukanidin E and Sleeman JP: Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol 22: 216-225, 2012.
34. Chen H, Fernig DG, Rudland PS, Sparks A, Wilkinson MC and Barraclough R: Binding to intracellular targets of the metastasis-inducing protein, S100A4 (p9Ka). Biochem Biophys Res Commun 286: 1212-1217, 2001. (Pubitemid 32924899)
35. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP and Lukanidin EM: Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269: 19679-19682, 1994. (Pubitemid 24250873)
36. Zimmer DB and Van Eldik LJ: Analysis of the calcium-modulated proteins, S100 and calmodulin, and their target proteins during C6 glioma cell differentiation. J Cell Biol 108: 141-151, 1989.
37. Zhao XQ, Naka M, Muneyuki M and Tanaka T: Ca(2+)-dependent inhibition of actin-activated myosin ATPase activity by S100C (S100A11), a novel member of the S100 protein family. Biochem Biophys Res Commun 267: 77-79, 2000. (Pubitemid 30072510)
38. Broome AM and Eckert RL: Microtubule-dependent redistribution of a cytoplasmic cornified envelope precursor. J Invest Dermatol 122: 29-38, 2004.
39. Hayes MJ, Shao D, Bailly M and Moss SE: Regulation of actin dynamics by annexin 2. EMBO J 25: 1816-1826, 2006.
40. de Graauw M, Tijdens I, Smeets MB et al: Annexin A2 phosphorylation mediates cell scattering and branching morphogenesis via cofilin activation. Mol Cell Biol 28: 1029-1040, 2008. (Pubitemid 351160059)
41. Rust RR, Baldisseri DM and Weber DJ: Structure of the negative regulatory domain of p53 bound to S100B (betabeta). Nat Struct Biol 7: 570-574, 2000. (Pubitemid 30445914)
42. Kato K, Kamada H, Fujimori T, Aritomo Y, Ono M and Masaki T: Molecular biologic approach to the diagnosis of pancreatic carcinoma using specimens obtained by EUS-guided fine needle aspiration. Gastroenterol Res Pract 2012: 243524, 2012.
43. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE and Chumakov PM: The antioxidant function of the p53 tumor suppressor. Nat Med 11: 1306-1313, 2005. (Pubitemid 41752911)
44. Green ML, Pisano MM, Prough RA and Knudsen TB: Release of targeted p53 from the mitochondrion as an early signal during mitochondrial dysfunction. Cell Signal 25: 2383-2390, 2013.
45. Leśniak W, Słomnicki LP and Filipek A: S100A6-new facts and features. Biochem Biophys Res Commun 390: 1087-1092, 2009.
46. Van Dieck J, Lum J K, Teufel D P and Fersht AR: S100 proteins interact with the N-terminal domain of MDM2. FEBS Letts 584: 3269-3274, 2010.
47. Wolf S, Haase-Kohn C and Pietzsch J: S100A2 in cancerogenesis: a friend or a foe? Amino Acids 41: 849-861, 2011.
48. Nishioku T, Furusho K, Tomita A, et al: Potential role for S100A4 in the disruption of the blood-brain barrier in collagen-induced arthritic mice, an animal model of rheumatoid arthritis. Neuroscience 189: 286-292, 2011.
49. Sapkota D, Costea DE, Blø M, Bruland O, Lorens JB, Vasstrand EN and Ibrahim SO: S100A14 inhibits proliferation of oral carcinoma derived cells through G1-arrest. Oral Oncol 48: 219-225, 2012.
50. Grigorian M, Andresen S, Tulchinsky E, et al: Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: functional consequences of their interaction. J Biol Chem 276: 22699-22708, 2001.
51. 2+/S100 proteins act as upstream regulators of the chaperone-associated ubiquitin ligase CHIP (C terminus of Hsc70-interacting protein). J Biol Chem 288: 7158-7168, 2013.
52. Romanov VS, Pospelov VA and Pospelova TV: Cyclin-dependent kinase inhibitor p21(Waf1): contemporary view on its role in senescence and oncogenesis. Biochemistry (Mosc.) 77: 575-584, 2012.
53. 2+)-induced growth inhibition of human epidermal keratinocytes. J Cell Biol 163: 825-835, 2003.
54. Li B, Wan X, Zhu Q, et al: Net expression inhibits the growth of pancreatic ductal adenocarcinoma cell PL45 in vitro and in vivo. PloS One 8: e57818, 2013.
55. Sakaguchi M and Huh NH: S100A11, a dual growth regulator of epidermal keratinocytes. Amino Acids 41: 797-807, 2011.
56. He H, Li J, Weng S, LI M and Yu Y: S100A11: diverse function and pathology corresponding to different target proteins. Cell Biochem Biophys 55: 117-126, 2009.
57. Ohuchida K, Mizumoto K, Ohhashi S, et al: S100A11, a putative tumor suppressor gene, is overexpressed in pancreatic carcinogenesis. Clin Cancer Res 12: 5417-5422, 2006. (Pubitemid 44497256)
58. Mann K and Hainaut P: Aminothiol WR1065 induces differential gene expression in the presence of wild-type p53. Oncogene 24: 3964-3975, 2005. (Pubitemid 40896408)
59. Brain JG, Robertson H, Thompson E, et al: Biliary epithelial senescence and plasticity in acute cellular rejection. Am J Transplant 13:1688-1702, 2013.
60. Yang SY, Miah A, Pabari A and Winslet M: Growth Factors and their receptors in cancer metastases. Front Biosci (Landmark Ed) 16: 531-538, 2011.
61. Jia W, Gao XJ, Yang ZX and Zhang ZD: S100A4 silencing suppresses proliferation, angiogenesis and invasion of thyroid cancer cells through downregulation of MMP-9 and VEGF. Eur Rev Med Pharmacol Sci 17: 1495-1508, 2013.
62. Chen H, Yuan Y, Zhang C, et al: Involvement of S100A14 protein in cell invasion by affecting expression and function of matrix metalloproteinase (MMP)-2 via p53-dependent transcriptional regulation. J Biol Chem 287: 17109-17119, 2012.
63. Gebhardt C, Németh J, Angel P and Hess J: S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72: 1622-1631, 2006. (Pubitemid 44666730)
64. Hsu TC, Young MR, Cmarik J and Colburn NH: Activator 1 (AP-1)- and nuclear factor kappaB (NF-kappaB)-dependent transcriptional events in carcinogenesis. Free Radic Biol Med 28: 1338-48, 2000. (Pubitemid 30621478)
65. Bachet JB, Maréchal R, Demetter P, et al: S100A2 is a predictive biomarker of adjuvant therapy benefit in pancreatic adenocarcinoma. Eur J Cancer 49: 2643-53, 2013.
66. Jamieson NB, Carter CR, McKay CJ and Oien KA: Tissue biomarkers for prognosis in pancreatic ductal adenocarcinoma: a systematic review and meta-analysis. Clin Cancer Res 17: 3316-3331, 2011.
67. Biankin AV, Kench JG, Colvin EK, et al: Expression of S100A2 calcium-binding protein predicts response to pancreatectomy for pancreatic cancer. Gastroenterology 137: 558-568, 2009.
68. Russo SM, Ove R and Saif MW: Identification of prognostic and predictive markers in pancreatic adenocarcinoma. Highlights from the '2011 ASCO Gastrointestinal Cancers Symposium'. San Francisco, CA, USA. January 20-22, 2011. JOP 12: 92-95, 2011.
69. Sekine H, Chen N, Sato K, et al: S100A4, frequently overexpressed in various human cancers, accelerates cell motility in pancreatic cancer cells. Biochem Biophys Res Commun 429: 214-219, 2012.
70. Ilg EC, Schäfer BW and Heizmann CW: Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68: 325-332, 1996. (Pubitemid 26384135)
71. Tsukamoto N, Egawa S, Akada M, et al: The expression of S100A4 in human pancreatic cancer is associated with invasion. Pancreas 42: 1027-1033, 2013.
72. Chang D, Colvin E, Scarlett C, et al: A molecular prognostic nomogram for resectable pancreatic cancer. J Clin Oncol 29 (Suppl 4): abs. 154, 2011.
73. Ikenaga N, Ohuchida K, Mizumoto K, et al: S100A4 mRNA is a diagnostic and prognostic marker in pancreatic carcinoma. J Gastrointest Surg 13: 1852-1858, 2009.
74. Schneider G and Filipek A: S100A6 binding protein and Siah-1 interacting protein (CacyBP/SIP): spotlight on properties and cellular function. Amino Acids 41: 773-780, 2011.
75. Ohuchida K, Mizumoto K, Ishikawa N, et al: The role of S100A6 in pancreatic cancer development and its clinical implication as a diagnostic marker and therapeutic target. Clin Cancer Res 11: 7785-7793, 2005. (Pubitemid 41611622)
76. Ohuchida K, Mizumoto K, Yu J, et al: S100A6 is increased in a stepwise manner during pancreatic carcinogenesis: clinical value of expression analysis in 98 pancreatic juice samples. Cancer Epidemiol Biomarkers Prev 16: 649-654, 2007. (Pubitemid 46650564)
77. Vimalachandran D, Greenhalf W, Thompson C, et al: High nuclear S100A6 (Calcyclin) is significantly associated with poor survival in pancreatic cancer patients. Cancer Res 65: 3218-3225, 2005. (Pubitemid 40524604)
78. Dowen SE, Crnogorac-Jurcevic T, Gangeswaran R, et al: Expression of S100P and its novel binding partner S100PBPR in early pancreatic cancer. Am J Pathol 166: 81-92, 2005. (Pubitemid 40051662)
79. Han H, Bearss DJ, Browne LW, Calaluce R, Nagle RB and Von Hoff DD: Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res 62: 2890-2896, 2002. (Pubitemid 34525776)
80. Ohuchida K, Mizumoto K, Egami T, et al: S100P is an early developmental marker of pancreatic carcinogenesis. Clin Cancer Res 12: 5411-5416, 2006. (Pubitemid 44497255)
81. Nakata K, Nagai E, Ohuchida K, et al: S100P is a novel marker to identify intraductal papillary mucinous neoplasms. Hum Pathol 41: 824-831, 2010.
82. 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. 201: 63-74, 2003. (Pubitemid 37121204)
83. Barry S, Chelala C, Lines K, et al: S100P is a metastasisassociated gene that facilitates transendothelial migration of pancreatic cancer cell. Clin Exp Metastasis 30: 251-264, 2013.
84. Inada H, Naka M, Tanaka T, Davey GE and Heizmann CW: Human S100A11 exhibits differential steady-state RNA levels in various tissues and a distinct subcellular localization. Biochem Biophys Res Commun 263: 135-138, 1999. (Pubitemid 29443652)
85. Chen JH, Ni RZ, Xiao MB, Guo JG and Zhou JW: Comparative proteomic analysis of differentially expressed proteins in human pancreatic cancer tissue. Hepatobiliary Pancreat Dis Int 8: 193-200, 2009.
86. Memon AA, Sorensen BS, Meldgaard P, Fokdal L, Thykjaer T and Nexo E: Down-regulation of S100C is associated with bladder cancer progression and poor survival. Clin Cancer Res 11: 606-611, 2005. (Pubitemid 40116886)
87. Nakashima T, Wang XF, Masuda M, Inokuchi A and Komiyama S: Overexpression of p53 nuclear protein in premalignant and malignant laryngeal lesions. Eur Arch Otorhinolaryngol 256: S56-S59, 1999. (Pubitemid 29201694)
88. Shin DM, Kim J, Ro JY, Hittelman J, Roth JA, Hong WK and Hittelman WN: Activation of p53 gene expression in premalignant lesions during head and neck tumorigenesis. Cancer Res 54: 321-326, 1994. (Pubitemid 24053159)
89. Xiao MB, Jiang F, Ni WK, Chen BY, Lu CH, Li XY and Ni RZ: High expression of S100A11 in pancreatic adenocarcinoma is an unfavorable prognostic marker. Med Oncol 29: 1886-1891, 2012.
90. Arumugam T, Simeone DM, Van Golen K and Logsdon CD: S100P promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res 11: 5356-5364, 2005. (Pubitemid 41060808)