RAGE mediates the pro-migratory response of extracellular S100A4 in human thyroid cancer cells

Thyroid

Volumn 25, Issue 5, 2015, Pages 514-527

  Medapati, Manoj Reddy ^a   Dahlmann, Mathias ^b   Ghavami, Saeid ^a,c   Pathak, Kumar Alok ^a   Lucman, Lydia ^d   Klonisch, Thomas ^a   Hoang Vu, Cuong ^e   Stein, Ulrike ^b   Hombach Klonisch, Sabine ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c CHILDREN S HOSPITAL RESEARCH INSTITUTE OF MANITOBA   (Canada)

^d ST BONIFACE GENERAL HOSPITAL   (Canada)

^e MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALVASCULIN; DIAPHANOUS 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ENZYME INHIBITOR; PROTEIN S 100; S100A4 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER TISSUE; CELL INVASION; CELL MIGRATION; CELL MIGRATION ASSAY; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; FLUORESCENCE IMAGING; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THYROID CANCER; WESTERN BLOTTING; ADENOCARCINOMA; CELL MOTION; DRUG EFFECTS; GENETICS; METABOLISM; PAPILLARY CARCINOMA; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; THYROID TUMOR; TUMOR CELL LINE;

ADENOCARCINOMA, FOLLICULAR; ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; CARCINOMA, PAPILLARY; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENZYME INHIBITORS; HUMANS; PROGNOSIS; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; S100 PROTEINS; SIGNAL TRANSDUCTION; THYROID NEOPLASMS;

EID: 84928895279     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2014.0257     Document Type: Article

References (59)

1. Kim HJ, Sung JY, Oh YL, Kim JH, Son YI, Min YK, Kim SW, Chung JH. (2014). Vascular invasion is associated with increased mortality in patients with minimally invasive follicular thyroid carcinoma but not widely invasive follicular thyroid carcinoma. Head Neck 36: 1695-1700
2. Passler C, Scheuba C, Prager G, Kaczirek K, Kaserer K, Zettinig G, Niederle B. (2004). Prognostic factors of papillary and follicular thyroid cancer: differences in an iodinereplete endemic goiter region. Endocr Relat Cancer 11: 131-139
3. Phay JE, Ringel MD. (2013). Metastatic mechanisms in follicular cell-derived thyroid cancer. Endocr Relat Cancer 20: R307-319
4. Chen M, Sinha M, Luxon BA, Bresnick AR, O'Connor KL. (2009). Integrin alpha6beta4 controls the expression of genes associated with cell motility, invasion, and metastasis, including S100A4/metastasin. J Biol Chem 284: 1484-1494
5. Jenkinson SR, Barraclough R, West CR, Rudland PS. (2004). S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer 90: 253-262
6. Sack U, Walther W, Scudiero D, Selby M, Aumann J, Lemos C, Fichtner I, Schlag PM, Shoemaker RH, Stein U. (2011). S100A4-induced cell motility and metastasis is restricted by the Wnt/beta-catenin pathway inhibitor calcimycin in colon cancer cells. Mol Biol Cell 22: 3344-3354
7. Stein U, Arlt F, Walther W, Smith J, Waldman T, Harris ED, Mertins SD, Heizmann CW, Allard D, Birchmeier W, Schlag PM, Shoemaker RH. (2006). The metastasis-Associated gene S100A4 is a novel target of beta-catenin/T-cell factor signaling in colon cancer. Gastroenterology 131: 1486-1500
8. 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. (2013). The expression of S100A4 in human pancreatic cancer is associated with invasion. Pancreas 42: 1027-1033
9. Zhang J, Zhang DL, Jiao XL, Dong Q. (2013). S100A4 regulates migration and invasion in hepatocellular carcinoma HepG2 cells via NF-kappaB-dependent MMP-9 signal. Eur Rev Med Pharmacol Sci 17: 2372-2382
10. Zou M, Famulski KS, Parhar RS, Baitei E, Al-Mohanna FA, Farid NR, Shi Y 2004Microarray analysis of metastasisassociated gene expression profiling in a murine model of thyroid carcinoma pulmonary metastasis: identification of S100A4 (Mts1) gene overexpression as a poor prognostic marker for thyroid carcinoma. J Clin Endocrinol Metab 89: 6146-6154
11. Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, Kobayashi K, Matsuzuka F, Kakudo K, Kuma K, Miyauchi A. (2004). S100A4 expression is an early event of papillary carcinoma of the thyroid. Oncology 67: 397-402
12. Min HS, Choe G, Kim SW, Park YJ, Park do J, Youn YK, Park SH, Cho BY, Park SY. (2008). S100A4 expression is associated with lymph node metastasis in papillary microcarcinoma of the thyroid. Mod Pathol 21: 748-755
13. Zou M, Al-Baradie RS, Al-Hindi H, Farid NR, Shi Y. (2005). S100A4 (Mts1) gene overexpression is associated with invasion and metastasis of papillary thyroid carcinoma. Br J Cancer 93: 1277-1284
14. Hombach-Klonisch S, Bialek J, Radestock Y, Truong A, Agoulnik AI, Fiebig B, Willing C, Weber E, Hoang-Vu C, Klonisch T. (2010). INSL3 has tumor-promoting activity in thyroid cancer. Int J Cancer 127: 521-531
15. Radestock Y, Willing C, Kehlen A, Hoang-Vu C, Hombach-Klonisch S. (2010). Relaxin enhances S100A4 and promotes growth of human thyroid carcinoma cell xenografts. Mol Cancer Res 8: 494-506
16. Ismail TM, Fernig DG, Rudland PS, Terry CJ, Wang G, Barraclough R. (2008). The basic C-Terminal amino acids of calcium-binding protein S100A4 promote metastasis. Carcinogenesis 29: 2259-2266
17. Kriajevska M, Fischer-Larsen M, Moertz E, Vorm O, Tulchinsky E, Grigorian M, Ambartsumian N, Lukanidin E. (2002). 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). J Biol Chem 277: 5229-5235
18. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP, Lukanidin EM. (1994). Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 269: 19679-19682
19. Zhang S, Wang G, Fernig DG, Rudland PS, Webb SE, Barraclough R, Barraclough R, Martin-Fernandez M. (2005). Interaction of metastasis-inducing S100A4 protein in vivo by fluorescence lifetime imaging microscopy. Eur Biophys J 34: 19-27
20. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ. (2010). HMGB1 and RAGE in inflammation and cancer. Ann Rev Immunol 28: 367-388
21. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tör M, Billiar T. (2007). The grateful dead: damage-Associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220: 60-81
22. Halayko AJ, Ghavami S. (2009). S100A8/A9: a mediator of severe asthma pathogenesis and morbidity? Can J Physiol Pharmacol 87: 743-755
23. Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ, Lotze MT. (2009). RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med 7: 17
24. Bierhaus A, Nawroth PP. (2009). Multiple levels of regulation determine the role of the receptor for AGE (RAGE) as common soil in inflammation, immune responses and diabetes mellitus and its complications. Diabetologia 52: 2251-2263
25. Fritz G. (2011). RAGE: a single receptor fits multiple ligands. Trends Biochem Sci 36: 625-632
26. Ghavami S, Chitayat S, Hashemi M, Eshraghi M, Chazin WJ, Halayko AJ, Kerkhoff C. (2009). S100A8/A9: a Janusfaced molecule in cancer therapy and tumorgenesis. Eur J Pharmacol 625: 73-83
27. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ, Hashemi M, Wesselborg S, Kerkhoff C, Los M. (2008). S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 83: 1484-1492
28. Hsieh HL, Schafer BW, Sasaki N, Heizmann CW. (2003). Expression analysis of S100 proteins and RAGE in human tumors using tissue microarrays. Biochem Biophys Res Commun 307: 375-381
29. Logsdon CD, Fuentes MK, Huang EH, Arumugam T. (2007). RAGE and RAGE ligands in cancer. Curr Mol Med 7: 777-789
30. Leclerc E, Fritz G, Vetter SW, Heizmann CW. (2009). Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 1793: 993-1007
31. Yammani RR, Long D, Loeser RF. (2009). Interleukin-7 stimulates secretion of S100A4 by activating the JAK/ STAT signaling pathway in human articular chondrocytes. Arthritis Rheum 60: 792-800
32. Hernández JL, Padilla L, Dakhel S, Coll T, Hervas R, Adan J, Masa M, Mitjans F, Martinez JM, Coma S, Rodríguez L, Noé V, Ciudad CJ, Blasco F, Messeguer R. (2013). Therapeutic targeting of tumor growth and angiogenesis with a novel anti-S100A4 monoclonal antibody. PloS One 8: e72480
33. Dahlmann M, Okhrimenko A, Marcinkowski P, Osterland M, Herrmann P, Smith J, Heizmann CW, Schlag PM, Stein U. (2014). RAGE mediates S100A4-induced cell motility via MAPK/ERK and hypoxia signaling and is a prognostic biomarker for human colorectal cancer metastasis. Oncotarget 5: 3220-3233
34. Siddique HR, Adhami VM, Parray A, Johnson JJ, Siddiqui IA, Shekhani MT, Murtaza I, Ambartsumian N, Konety BR, Mukhtar H, Saleem M. (2013). The S100A4 oncoprotein promotes prostate tumorigenesis in a transgenic mouse model: regulating NFjB through the RAGE receptor. Genes Cancer 4: 224-234
35. Glogowska A, Kunanuvat U, Stetefeld J, Patel TR, Thanasupawat T, Krcek J, Weber E, Wong GW, Del Bigio MR, Hoang-Vu C, Hombach-Klonisch S, Klonisch T. (2013). C1qtumor necrosis factor-related protein 8 (CTRP8) is a novel interaction partner of relaxin receptor RXFP1 in human brain cancer cells. J Pathol 231: 466-479
36. Yammani RR, Carlson CS, Bresnick AR, Loeser RF. (2006). Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: role of the receptor for advanced glycation end products. Arthritis Rheum 54: 2901-2911
37. Hansen MT, Forst B, Cremers N, Quagliata L, Ambartsumian N, Grum-Schwensen B, Klingelhöfer J, Abdul-Al A, Herrmann P, Osterland M, Stein U, Nielsen GH, Scherer PE, Lukanidin E, Sleeman JP, Grigorian M. (2015). A link between inflammation and metastasis: serum amyloid A1 and A3 induce metastasis, and are targets of metastasisinducing S100A4. Oncogene 34: 424-435
38. Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, D'Agati V, Schmidt AM. (2008). Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J Biol Chem 283: 34457-34468
39. Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A. (2007). 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
40. Ostendorp T, Leclerc E, Galichet A, Koch M, Demling N, Weigle B, Heizmann CW, Kroneck PMH, Günter F. (2007). Structural and functional insights into RAGE activation by multimeric S100B. EMBO J 26: 3868-3878
41. Semov A, Moreno MJ, Onichtchenko A, Abulrob A, Ball M, Ekiel I, Pietrzynski G, Stanimirovic D, Alakhov V. (2005). Metastasis-Associated protein S100A4 induces angiogenesis through interaction with Annexin II and accelerated plasmin formation. J Biol Chem 280: 20833-20841
42. Kiryushko D, Novitskaya V, Soroka V, Klingelhöfer J, Lukanidin E, Berezin V, Bock E. (2006). Molecular mechanisms of Ca(2 + ) signaling in neurons induced by the S100A4 protein. Mol Cell Biol 26: 3625-3638
43. Breitenlechner C, Gassel M, Hidaka H, Kinzel V, Huber R, Engh RA, Bossemeyer D. (2003). Protein kinase A in complex with Rho-kinase inhibitors Y-27632, Fasudil, and H-1152P: structural basis of selectivity. Structure 11: 1595-1607
44. Ikenoya M, Hidaka H, Hosoya T, Suzuki M, Yamamoto N, Sasaki Y. (2002). Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor. J Neurochem 81: 9-16
45. Tkachenko E, Sabouri-Ghomi M, Pertz O, Kim C, Gutierrez E, Machacek M, Groisman A, Danuser G, Ginsberg MH. (2011). Protein kinase A governs a RhoA-RhoGDI protrusion-retraction pacemaker in migrating cells. Nature Cell Biol 13: 660-667
46. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, Van Der Poll T, Sorg C, Roth J. (2007). Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13: 1042-1049
47. Bochet L, Lehuede C, Dauvillier S, Wang YY, Dirat B, Laurent V, Dray C, Guiet R, Maridonneau-Parini I, Le Gonidec S, Couderc B, Escourrou G, Valet P, Muller C. (2013). Adipocyte-derived fibroblasts promote tumor progression and contribute to the desmoplastic reaction in breast cancer. Cancer Res 73: 5657-5668
48. Rasanen K, Sriswasdi S, Valiga A, Tang HY, Zhang G, Perego M, Somasundaram R, Li L, Speicher K, Klein-Szanto AJ, Basu D, Rustgi AK, Speicher DW, Herlyn M. (2013). Comparative secretome analysis of epithelial and mesenchymal subpopulations of head and neck squamous cell carcinoma identifies S100A4 as a potential therapeutic target. Mol Cell Proteomics 12: 3778-3792
49. Cabezón T, Celis JE, Skibshøj I, Klingelhöfer J, Grigorian M, Gromov P, Rank F, Myklebust JH, Maelandsmo GM, Lukanidin E, Ambartsumian N. (2007). Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int J Cancer 121: 1433-1444
50. Ambartsumian N, Klingelhöfer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E, Georgiev G, Berezin V, Bock E, Rygaard J, Cao R, Cao Y, Lukanidin E. (2001). The metastasis-Associated Mts1(S100A4) protein could act as an angiogenic factor. Oncogene 20: 4685-4695
51. Koch M, Chitayat S, Dattilo BM, Schiefner A, Diez J, Chazin WJ, Fritz G. (2010). Structural basis for ligand recognition and activation of RAGE. Structure 18: 1342-1352
52. Huttunen HJ, Rauvala H. (2004). Amphoterin as an extracellular regulator of cell motility: from discovery to disease. J Intern Med 255: 351-366
53. Jin Q, Chen H, Luo A, Ding F, Liu Z. (2011). S100A14 stimulates cell proliferation and induces cell apoptosis at different concentrations via receptor for advanced glycation end products (RAGE). PloS One 6: e19375
54. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY. (2004). Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 164: 1389-1397
55. Reeb AN, Li W, Sewell W, Marlow LA, Tun HW, Smallridge RC, Copland JA, Spradling K, Chernock R, Lin RY. (2015). S100A8 is a novel therapeutic target for anaplastic thyroid carcinoma. J Clin Endocrinol Metab 100: E232-E242
56. Spiekerkoetter E, Guignabert C, de Jesus Perez V, Alastalo TP, Powers JM, Wang L, Lawrie A, Ambartsumian N, Schmidt AM, Berryman M, Ashley RH, Rabinovitch M. (2009). S100A4 and bone morphogenetic protein-2 codependently induce vascular smooth muscle cell migration via phospho-extracellular signal-regulated kinase and chloride intracellular channel 4. Circ Res 105: 639-647, 13 p following 47
57. Klingelhöfer J, Moller HD, Sumer EU, Berg CH, Poulsen M, Kiryushko D, Soroka V, Ambartsumian N, Grigorian M, Lukanidin EM. (2009). Epidermal growth factor receptor ligands as new extracellular targets for the metastasispromoting S100A4 protein. FEBS J 276: 5936-5948
58. Schmidt AM, Yan SD, Yan SF, Stern DM. (2001). The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108: 949-955
59. Bozec A, Lassalle S, Hofman V, Ilie M, Santini J, Hofman P. (2010). The thyroid gland: a crossroad in inflammationinduced carcinoma? An ongoing debate with new therapeutic potential. Curr Med Chem 17: 3449-3461