S100 family signaling network and related proteins in pancreatic cancer (Review)
- Authors:
- Yi-Fei Ji
- Hua Huang
- Feng Jiang
- Run-Zhou Ni
- Ming-Bing Xiao
-
Affiliations: Department of Gastroenterology, Affiliated Hospital of Nantong University, Nantong, Jiangsu 226001, P.R. China, Department of Pathology, Affiliated Hospital of Nantong University, Nantong, Jiangsu 226001, P.R. China - Published online on: January 24, 2014 https://doi.org/10.3892/ijmm.2014.1633
- Pages: 769-776
This article is mentioned in:
Abstract
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.PubMed/NCBI | |
Arumugam T and Logsdon CD: S100P: a novel therapeutic target for cancer. Amino acids. 41:893–899. 2011. View Article : Google Scholar | |
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 significances of tissue and serum galectin-3 in pancreatic carcinoma. J Cancer Res Clin Oncol. 138:1035–1043. 2012. View Article : Google Scholar : PubMed/NCBI | |
Danovi SA, Wong HH and Lemoine NR: Targeted therapies for pancreatic cancer. Br Med Bull. 87:97–130. 2008. View Article : Google Scholar : PubMed/NCBI | |
Rezvanpour A and Shaw GS: Unique S100 target protein interactions. Gen Physiol Biophys. 28:F39–F46. 2009. | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Moore BW: A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun. 19:739–744. 1965. View Article : Google Scholar : PubMed/NCBI | |
Zimmer DB, Cornwall EH, Landar A and Song W: The S100 protein family: history, function, and expression. Brain Res Bull. 37:417–429. 1995. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Melle C, Ernst G, Schimmel B, Bleul A and Eggeling FV: Colon-derived liver metastasis, colorectal carcinoma, and hepatocellular carcinoma can be discriminated by the Ca(2+)-binding proteins S100A6 and S100A11. PloS One. 3:e37672008. View Article : Google Scholar : PubMed/NCBI | |
Schäfer BW and Heizmann CW: The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci. 21:134–140. 1996.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Heizmann CW, Ackermann GE and Galichet A: Pathologies involving the S100 proteins and RAGE. Subcell Biochem. 45:93–138. 2007. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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). | |
Sorci G, Riuzzi F, Giambanco I and Donato R: RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta. 1833:101–109. 2012. View Article : Google Scholar | |
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. View Article : Google Scholar : PubMed/NCBI | |
Maletzki C, Bodammer P, Breitrück A and Kerkhoff C: S100 proteins as diagnostic and prognostic markers in colorectal and hepatocellular carcinoma. Hepat Mon. 12:e72402012.PubMed/NCBI | |
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. 107:2502012.PubMed/NCBI | |
Hung KW, Chang YM and Yu C: Resonance assignments of Ca2+-bound human S100A11. Biomol NMR Assign. 7:211–214. 2013. View Article : Google Scholar | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Leclerc E and Heizmann CW: The importance of Ca2+/Zn2+ signaling S100 proteins and RAGE in translational medicine. Front Biosci (Schol Ed). 3:1232–1262. 2011. | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Taguchi A, Blood DC, del Toro G, et al: Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 405:354–360. 2000. View Article : Google Scholar : PubMed/NCBI | |
Lukanidin E and Sleeman JP: Building the niche: the role of the S100 proteins in metastatic growth. Semin Cancer Biol. 22:216–225. 2012. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. | |
Broome AM and Eckert RL: Microtubule-dependent redistribution of a cytoplasmic cornified envelope precursor. J Invest Dermatol. 122:29–38. 2004. View Article : Google Scholar : PubMed/NCBI | |
Hayes MJ, Shao D, Bailly M and Moss SE: Regulation of actin dynamics by annexin 2. EMBO J. 25:1816–1826. 2006. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. 2012:2435242012. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Leśniak W, Słomnicki LP and Filipek A: S100A6-new facts and features. Biochem Biophys Res Commun. 390:1087–1092. 2009. | |
Van Dieck J, Lum JK and Fersht AR: S100 proteins interact with the N-terminal domain of MDM2. FEBS Letts. 584:3269–3274. 2010.PubMed/NCBI | |
Wolf S, Haase-Kohn C and Pietzsch J: S100A2 in cancerogenesis: a friend or a foe? Amino Acids. 41:849–861. 2011. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Shimamoto S, Kubota Y, Yamaguchi F, Tokumitsu H and Kobayashi R: Ca2+/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. | |
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. View Article : Google Scholar : PubMed/NCBI | |
Sakaguchi M, Miyazaki M, Takaishi M, et al: S100C/A11 is a key mediator of Ca(2+)-induced growth inhibition of human epidermal keratinocytes. J Cell Biol. 163:825–835. 2003.PubMed/NCBI | |
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:e578182013. View Article : Google Scholar : PubMed/NCBI | |
Sakaguchi M and Huh NH: S100A11, a dual growth regulator of epidermal keratinocytes. Amino Acids. 41:797–807. 2011. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Mann K and Hainaut P: Aminothiol WR1065 induces differential gene expression in the presence of wild-type p53. Oncogene. 24:3964–3975. 2005. View Article : Google Scholar : PubMed/NCBI | |
Brain JG, Robertson H, Thompson E, et al: Biliary epithelial senescence and plasticity in acute cellular rejection. Am J Transplant. 13:1688–1702. 2013. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Gebhardt C, Németh J, Angel P and Hess J: S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol. 72:1622–1631. 2006. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Russo SM, Ove R and Saif MW: Identification of prognostic and predictive markers in pancreatic adenocarcinoma. In: Highlights from the ‘2011 ASCO Gastrointestinal Cancers Sympsoium’; San Francisco, CA, USA. January 20–22, 2011; JOP. 12. pp. 92–95. 2011, PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Ilg EC, Schäfer BW and Heizmann CW: Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer. 68:325–332. 1996. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
Ohuchida K, Mizumoto K, Egami T, et al: S100P is an early developmental marker of pancreatic carcinogenesis. Clin Cancer Res. 12:5411–5416. 2006. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar | |
Barry S, Chelala C, Lines K, et al: S100P is a metastasis-associated gene that facilitates transendothelial migration of pancreatic cancer cell. Clin Exp Metastasis. 30:251–264. 2013. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI |