The role of S100 proteins and their receptor RAGE in pancreatic cancer

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 12, 2015, Pages 2706-2711

  Leclerc, Estelle ^a   Vetter, Stefan W ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Pancreatic ductal adenocarcinoma; RAGE; S100 proteins

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; CALCYCLIN; CALGRANULIN A; CALGRANULIN B; CALVASCULIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; FLUOROURACIL; FOLINIC ACID; GEMCITABINE; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; OXALIPLATIN; PROTEIN KINASE B; PROTEIN P53; PROTEIN PATCHED 1; PROTEIN S 100; PROTEIN S100A11; PROTEIN S100A2; PROTEIN S100P; REACTIVE OXYGEN METABOLITE; SMAD4 PROTEIN; SONIC HEDGEHOG PROTEIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR GLI1; UNCLASSIFIED DRUG;

AUTOPHAGY; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; NONHUMAN; ONCOGENE K RAS; OXIDATIVE STRESS; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR SUPPRESSOR GENE;

EID: 84943619619     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.09.022     Document Type: Review

References (50)

1. Fokas E., O'Neill E., Gordon-Weeks A., Mukherjee S., McKenna W.G., Muschel R.J. Pancreatic ductal adenocarcinoma: from genetics to biology to radiobiology to oncoimmunology and all the way back to the clinic. Biochim. Biophys. Acta 2015, 1855:61-82.
2. DiNorcia J., Lee M.K., Moroziewicz D.N., Winner M., Suman P., Bao F., Remotti H.E., Zou Y.S., Yan S.F., Qiu W., Su G.H., Schmidt A.M., Allendorf J.D. RAGE gene deletion inhibits the development and progression of ductal neoplasia and prolongs survival in a murine model of pancreatic cancer. J. Gastrointest. Surg. 2012, 16:104-112.
3. Donato R., Cannon B.R., Sorci G., Riuzzi F., Hsu K., Weber D.J., Geczy C.L. Functions of S100 proteins. Curr. Mol. Med. 2013, 13:24-57.
4. Riehl A., Nemeth J., Angel P., Hess J. The receptor RAGE: bridging inflammation and cancer. Cell Commun. Signal 2009, 7:12.
5. Fritz G. RAGE: a single receptor fits multiple ligands. Trends Biochem. Sci. 2011, 36:625-632.
6. Hudson B.I., Carter A.M., Harja E., Kalea A.Z., Arriero M., Yang H., Grant P.J., Schmidt A.M. Identification, classification, and expression of RAGE gene splice variants. FASEB J. 2008, 22:1572-1580.
7. Arumugam T., Ramachandran V., Sun D., Peng Z., Pal A., Maxwell D.S., Bornmann W.G., Logsdon C.D. Designing and developing S100P inhibitor 5-methyl cromolyn for pancreatic cancer therapy. Mol. Cancer Ther. 2013, 12:654-662.
8. Kang R., Tang D., Schapiro N.E., Loux T., Livesey K.M., Billiar T.R., Wang H., Van Houten B., Lotze M.T., Zeh H.J. The HMGB1/RAGE inflammatory pathway promotes pancreatic tumor growth by regulating mitochondrial bioenergetics. Oncogene 2014, 33:567-577.
9. Kondratska K., Kondratskyi A., Yassine M., Lemonnier L., Lepage G., Morabito A., Skryma R., Prevarskaya N. Orai1 and STIM1 mediate SOCE and contribute to apoptotic resistance of pancreatic adenocarcinoma. Biochim. Biophys. Acta 2014, 1843:2263-2269.
10. Fritz G., Heizmann C.W. 3D structures of the calcium and zinc binding s100 proteins. Encyclopedia of Inorganic and Bioinorganic Chemistry 2011, Wiley Online Library. J.W. Sons (Ed.).
11. Bresnick A.R., Weber D.J., Zimmer D.B. S100 proteins in cancer. Nat. Rev. Cancer 2015, 15:96-109.
12. Gross S.R., Sin C.G., Barraclough R., Rudland P.S. Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell. Mol. Life Sci. 2014, 71:1551-1579.
13. Bachet J.B., Marechal R., Demetter P., Bonnetain F., Cros J., Svrcek M., Bardier-Dupas A., Hammel P., Sauvanet A., Louvet C., Paye F., Vaillant J.C., Andre T., Closset J., Salmon I., Emile J.F., Van Laethem J.L. S100A2 is a predictive biomarker of adjuvant therapy benefit in pancreatic adenocarcinoma. Eur. J. Cancer 2013, 49:2643-2653.
14. Jamieson N.B., Denley S.M., Logue J., MacKenzie D.J., Foulis A.K., Dickson E.J., Imrie C.W., Carter R., McKay C.J., McMillan D.C. A prospective comparison of the prognostic value of tumor- and patient-related factors in patients undergoing potentially curative surgery for pancreatic ductal adenocarcinoma. Ann. Surg. Oncol. 2011, 18:2318-2328.
15. Leclerc E., Fritz G., Vetter S.W., Heizmann C.W. Binding of S100 proteins to RAGE: an update. Biochim. Biophys. Acta 2009, 1793:993-1007.
16. Nutter F., Holen I., Brown H.K., Cross S.S., Evans C.A., Walker M., Coleman R.E., Westbrook J.A., Selby P.J., Brown J.E., Ottewell P.D. Different molecular profiles are associated with breast cancer cell homing compared with colonisation of bone: evidence using a novel bone-seeking cell line. Endocr. Relat. Cancer 2014, 21:327-341.
17. Sekine H., Chen N., Sato K., Saiki Y., Yoshino Y., Umetsu Y., Jin G., Nagase H., Gu Z., Fukushige S., Sunamura M., Horii A. S100A4, frequently overexpressed in various human cancers, accelerates cell motility in pancreatic cancer cells. Biochem. Biophys. Res. Commun. 2012, 429:214-219.
18. Kozono S., Ohuchida K., Ohtsuka T., Cui L., Eguchi D., Fujiwara K., Zhao M., Mizumoto K., Tanaka M. S100A4 mRNA expression level is a predictor of radioresistance of pancreatic cancer cells. Oncol. Rep. 2013, 30:1601-1608.
19. Tsukamoto N., Egawa S., Akada M., Abe K., Saiki Y., Kaneko N., Yokoyama S., Shima K., Yamamura A., Motoi F., Abe H., Hayashi H., Ishida K., Moriya T., Tabata T., Kondo E., Kanai N., Gu Z., Sunamura M., Unno M., Horii A. The expression of S100A4 in human pancreatic cancer is associated with invasion. Pancreas 2013, 42:1027-1033.
20. Lee S.H., Kim H., Hwang J.H., Shin E., Lee H.S., Hwang D.W., Cho J.Y., Yoon Y.S., Han H.S., Cha B.H. CD24 and S100A4 expression in resectable pancreatic cancers with earlier disease recurrence and poor survival. Pancreas 2014, 43:380-388.
21. Dahlmann M., Okhrimenko A., Marcinkowski P., Osterland M., Herrmann P., Smith J., Heizmann C.W., Schlag P.M., Stein U. RAGE mediates S100A4-induced cell motility via MAPK/ERK and hypoxia signaling and is a prognostic biomarker for human colorectal cancer metastasis. Oncotarget 2014, 5:3220-3233.
22. Siddique H.R., Adhami V.M., Parray A., Johnson J.J., Siddiqui I.A., Shekhani M.T., Murtaza I., Ambartsumian N., Konety B.R., Mukhtar H., Saleem M. The S100A4 oncoprotein promotes prostate tumorigenesis in a transgenic mouse model: regulating NFkappaB through the RAGE receptor. Genes Cancer 2013, 4:224-234.
23. Haase-Kohn C., Wolf S., Herwig N., Mosch B., Pietzsch J. Metastatic potential of B16-F10 melanoma cells is enhanced by extracellular S100A4 derived from RAW264.7 macrophages. Biochem. Biophys. Res. Commun. 2014, 446:143-148.
24. Xu X., Su B., Xie C., Wei S., Zhou Y., Liu H., Dai W., Cheng P., Wang F., Xu X., Guo C. Sonic hedgehog-Gli1 signaling pathway regulates the epithelial mesenchymal transition (EMT) by mediating a new target gene, S100A4, in pancreatic cancer cells. PLoS One 2014, 9.
25. Che P., Yang Y., Han X., Hu M., Sellers J.C., Londono-Joshi A.I., Cai G.Q., Buchsbaum D.J., Christein J.D., Tang Q., Chen D., Li Q., Grizzle W.E., Lu Y.Y., Ding Q. S100A4 promotes pancreatic cancer progression through a dual signaling pathway mediated by Src and focal adhesion kinase. Sci. Rep. 2015, 5:8453-8463.
26. Zihao G., Jie Z., Yan L., Jing Z., Jing C., Xue L., Jing Z., Heng L.W., Ru G., Jianyu H. Analyzing S100A6 expression in endoscopic ultrasonography-guided fine-needle aspiration specimens: a promising diagnostic method of pancreatic cancer. J. Clin. Gastroenterol. 2013, 47:69-75.
27. Chen X., Liu X., Lang H., Zhang S., Luo Y., Zhang J. S100 Calcium-binding protein A6 promotes epithelial-mesenchymal transition through beta-catenin in pancreatic cancer cell line. PLoS One 2015, 10.
28. Mohan S.K., Gupta A.A., Yu C. Interaction of the S100A6 mutant (C3S) with the V domain of the receptor for advanced glycation end products (RAGE). Biochem. Biophys. Res. Commun. 2013, 434:328-333.
29. Jurewicz E., Goral A., Filipek A. S100A6 is secreted from Wharton's jelly mesenchymal stem cells and interacts with integrin beta1. Int. J. Biochem. Cell Biol. 2014, 55:298-303.
30. Arumugam T., Logsdon C.D. S100P: a novel therapeutic target for cancer. Amino Acids 2011, 41:893-899.
31. Ali A., Brown V., Denley S., Jamieson N.B., Morton J.P., Nixon C., Graham J.S., Sansom O.J., Carter C.R., McKay C.J., Duthie F.R., Oien K.A. Expression of KOC, S100P, mesothelin and MUC1 in pancreatico-biliary adenocarcinomas: development and utility of a potential diagnostic immunohistochemistry panel. BMC Clin. Pathol. 2014, 14:35.
32. Hu H., Zhang Q., Huang C., Shen Y., Chen X., Shi X., Tang W. Diagnostic value of S100P for pancreatic cancer: a meta-analysis. Tumour Biol. 2014, 35:9479-9485.
33. Penumutchu S.R., Chou R.H., Yu C. Structural insights into calcium-bound S100P and the V domain of the RAGE complex. PLoS One 2014, 9.
34. Arumugam T., Ramachandran V., Gomez S.B., Schmidt A.M., Logsdon C.D. S100P-derived RAGE antagonistic peptide reduces tumor growth and metastasis. Clin. Cancer Res. 2012, 18:4356-4364.
35. Penumutchu S.R., Chou R.H., Yu C. Interaction between S100P and the anti-allergy drug cromolyn. Biochem. Biophys. Res. Commun. 2014, 454:404-409.
36. Kim C.E., Lim S.K., Kim J.S. In vivo antitumor effect of cromolyn in PEGylated liposomes for pancreatic cancer. J. Control. Release 2012, 157:190-195.
37. Dakhel S., Padilla L., Adan J., Masa M., Martinez J.M., Roque L., Coll T., Hervas R., Calvis C., Messeguer R., Mitjans F., Hernandez J.L. S100P antibody-mediated therapy as a new promising strategy for the treatment of pancreatic cancer. Oncogenesis 2014, 3.
38. Yin C., Li H., Zhang B., Liu Y., Lu G., Lu S., Sun L., Qi Y., Li X., Chen W. RAGE-binding S100A8/A9 promotes the migration and invasion of human breast cancer cells through actin polymerization and epithelial-mesenchymal transition. Breast Cancer Res. Treat. 2013, 142:297-309.
39. Hiratsuka S., Ishibashi S., Tomita T., Watanabe A., Akashi-Takamura S., Murakami M., Kijima H., Miyake K., Aburatani H., Maru Y. Primary tumours modulate innate immune signalling to create pre-metastatic vascular hyperpermeability foci. Nat. Commun. 2013, 4:1853.
40. Sheikh A.A., Vimalachandran D., Thompson C.C., Jenkins R.E., Nedjadi T., Shekouh A., Campbell F., Dodson A., Prime W., Crnogorac-Jurcevic T., Lemoine N.R., Costello E. The expression of S100A8 in pancreatic cancer-associated monocytes is associated with the Smad4 status of pancreatic cancer cells. Proteomics 2007, 7:1929-1940.
41. Basso D., Greco E., Padoan A., Fogar P., Scorzeto M., Fadi E., Bozzato D., Moz S., Navaglia F., Zambon C.F., Seraglia R., De Carlo E., Valerio A., Reggiani C., Pedrazzoli S., Plebani M. Altered intracellular calcium fluxes in pancreatic cancer induced diabetes mellitus: relevance of the S100A8 N-terminal peptide (NT-S100A8). J. Cell. Physiol. 2011, 226:456-468.
42. Jones S., Zhang X., Parsons D.W., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Kamiyama H., Jimeno A., Hong S.M., Fu B., Lin M.T., Calhoun E.S., Kamiyama M., Walter K., Nikolskaya T., Nikolsky Y., Hartigan J., Smith D.R., Hidalgo M., Leach S.D., Klein A.P., Jaffee E.M., Goggins M., Maitra A., Iacobuzio-Donahue C., Eshleman J.R., Kern S.E., Hruban R.H., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806.
43. Ang C.W., Nedjadi T., Sheikh A.A., Tweedle E.M., Tonack S., Honap S., Jenkins R.E., Park B.K., Schwarte-Waldhoff I., Khattak I., Azadeh B., Dodson A., Kalirai H., Neoptolemos J.P., Rooney P.S., Costello E. Smad4 loss is associated with fewer S100A8-positive monocytes in colorectal tumors and attenuated response to S100A8 in colorectal and pancreatic cancer cells. Carcinogenesis 2010, 31:1541-1551.
44. Basso D., Fogar P., Plebani M. The S100A8/A9 complex reduces CTLA4 expression by immature myeloid cells: implications for pancreatic cancer-driven immunosuppression. Oncoimmunology 2013, 2.
45. Kallberg E., Vogl T., Liberg D., Olsson A., Bjork P., Wikstrom P., Bergh A., Roth J., Ivars F., Leanderson T. S100A9 interaction with TLR4 promotes tumor growth. PLoS One 2012, 7.
46. D. Basso, D. Bozzato, A. Padoan, S. Moz, C.F. Zambon, P. Fogar, E. Greco, M. Scorzeto, F. Simonato, F. Navaglia, M. Fassan, M. Pelloso, S. Dupont, S. Pedrazzoli, A. Fassina, M. Plebani, Inflammation and pancreatic cancer: molecular and functional interactions between S100A8, S100A9, NT-S100A8 and TGFbeta1, Cell Commun. Signal, 12 (2014) 20.
47. Chen K.T., Kim P.D., Jones K.A., Devarajan K., Patel B.B., Hoffman J.P., Ehya H., Huang M., Watson J.C., Tokar J.L., Yeung A.T. Potential prognostic biomarkers of pancreatic cancer. Pancreas 2014, 43:22-27.
48. Ohuchida K., Mizumoto K., Ohhashi S., Yamaguchi H., Konomi H., Nagai E., Yamaguchi K., Tsuneyoshi M., Tanaka M. S100A11, a putative tumor suppressor gene, is overexpressed in pancreatic carcinogenesis. Clin. Cancer Res. 2006, 12:5417-5422.
49. Xiao M.B., Jiang F., Ni W.K., Chen B.Y., Lu C.H., Li X.Y., Ni R.Z. High expression of S100A11 in pancreatic adenocarcinoma is an unfavorable prognostic marker. Med. Oncol. 2012, 29:1886-1891.
50. Burstein A.H., Grimes I., Galasko D.R., Aisen P.S., Sabbagh M., Mjalli A.M. Effect of TTP488 in patients with mild to moderate Alzheimer's disease. BMC Neurol. 2014, 14:12.