S100A9 promotes human hepatocellular carcinoma cell growth and invasion through RAGE-mediated ERK1/2 and p38 MAPK pathways

Experimental Cell Research

Volumn 334, Issue 2, 2015, Pages 228-238

  Wu, Rui ^a   Duan, Liang ^b   Cui, Fang ^a   Cao, Ju ^a   Xiang, Yu ^a   Tang, Yishu ^a   Zhou, Lan ^b  

^a THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Growth; Hepatocellular carcinoma; Invasion; S100A9

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; EPITHELIAL CELL ADHESION MOLECULE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN S 100; PROTEIN S 100A9; UNCLASSIFIED DRUG; ADVANCED GLYCOSYLATION END-PRODUCT RECEPTOR; CALGRANULIN B; IMMUNOGLOBULIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL INVASION; CELL SURVIVAL; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; ELECTROPHORESIS; FEMALE; GENE EXPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VIVO STUDY; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; NUCLEAR SHAPE; NUCLEAR SIZE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RANDOMIZED CONTROLLED TRIAL; SIGNAL TRANSDUCTION; TUMOR DIFFERENTIATION; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; DISEASE MODEL; EXPERIMENTAL LIVER NEOPLASM; HEPG2 CELL LINE; LIVER TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR INVASION;

ANIMALS; CALGRANULIN B; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM INVASIVENESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, IMMUNOLOGIC;

EID: 84929518260     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.04.008     Document Type: Article

References (59)

1. El-Serag H.B. Hepatocellular carcinoma. N. Engl. J. Med. 2011, 365:1118-1127.
2. Kremsdorf D., Soussan P., Paterlini-Brechot P., Brechot C. Hepatitis B virus-related hepatocellular carcinoma: paradigms for viral-related human carcinogenesis. Oncogene 2006, 25:3823-3833.
3. Nakamoto Y., Guidotti L.G., Kuhlen C.V., Fowler P., Chisari F.V. Immune pathogenesis of hepatocellular carcinoma. J. Exp. Med. 1998, 188:341-350.
4. Thorgeirsson S.S., Grisham J.W. Molecular pathogenesis of human hepatocellular carcinoma. Nat. Genet. 2002, 31:339-346.
5. Farazi P.A., DePinho R.A. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat. Rev. Cancer 2006, 6:674-687.
6. Ding J., Wang H. Multiple interactive factors in hepatocarcinogenesis. Cancer Lett. 2014, 346:17-23.
7. Szabo G., Lippai D. Molecular hepatic carcinogenesis: impact of inflammation. Dig. Dis. 2012, 30:243-248.
8. Chazin W.J. Relating form and function of EF-hand calcium binding proteins. Acc. Chem. Res. 2011, 44:171-179.
9. Lackmann M., Rajasekariah P., Iismaa S.E., Jones G., Cornish C.J., Hu S., Simpson R.J., Moritz R.L., Geczy C.L. Identification of a chemotactic domain of the pro-inflammatory S100 protein CP-10. J. Immunol. 1993, 150:2981-2991.
10. Benedyk M., Sopalla C., Nacken W., Bode G., Melkonyan H., Banfi B., Kerkhoff C. HaCaT keratinocytes overexpressing the S100 proteins S100A8 and S100A9 show increased NADPH oxidase and NF-kappaB activities. J. Investig. Dermatol. 2007, 127:2001-2011.
11. Markowitz J., Carson W.R. Review of S100A9 biology and its role in cancer. Biochim. Biophys. Acta 1835, 2013:100-109.
12. Ghavami S., Rashedi I., Dattilo B.M., Eshraghi M., Chazin W.J., Hashemi M., Wesselborg S., Kerkhoff C., Los M. S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J. Leukoc. Biol. 2008, 83:1484-1492.
13. Hermani A., De Servi B., Medunjanin S., Tessier P.A., Mayer D. S100A8 and S100A9 activate MAP kinase and NF-kappaB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp. Cell Res. 2006, 312:184-197.
14. Choi D.K., Li Z.J., Chang I.K., Yeo M.K., Kim J.M., Sohn K.C., Im M., Seo Y.J., Lee J.H., Kim C.D., Lee Y. Clinicopathological roles of S100A8 and S100A9 in cutaneous squamous cell carcinoma in vivo and in vitro. Arch. Dermatol. Res. 2014, 306:489-496.
15. Arai K., Yamada T., Nozawa R. Immunohistochemical investigation of migration inhibitory factor-related protein (MRP)-14 expression in hepatocellular carcinoma. Med. Oncol. 2000, 17:183-188.
16. Nemeth J., Stein I., Haag D., Riehl A., Longerich T., Horwitz E., Breuhahn K., Gebhardt C., Schirmacher P., Hahn M., Ben-Neriah Y., Pikarsky E., Angel P., Hess J. S100A8 and S100A9 are novel nuclear factor kappa B target genes during malignant progression of murine and human liver carcinogenesis. Hepatology 2009, 50:1251-1262.
17. Wu R., Duan L., Ye L., Wang H., Yang X., Zhang Y., Chen X., Zhang Y., Weng Y., Luo J., Tang M., Shi Q., He T., Zhou L. S100A9 promotes the proliferation and invasion of HepG2 hepatocellular carcinoma cells via the activation of the MAPK signaling pathway. Int. J. Oncol. 2013, 42:1001-1010.
18. Riehl A., Nemeth J., Angel P., Hess J. The receptor RAGE: bridging inflammation and cancer, Cell Commun. Signal 2009, 7:12.
19. Taguchi A., Blood D.C., del T.G., Canet A., Lee D.C., Qu W., Tanji N., Lu Y., Lalla E., Fu C., Hofmann M.A., Kislinger T., Ingram M., Lu A., Tanaka H., Hori O., Ogawa S., Stern D.M., Schmidt A.M. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000, 405:354-360.
20. Hiwatashi K., Ueno S., Abeyama K., Kubo F., Sakoda M., Maruyama I., Hamanoue M., Natsugoe S., Aikou T. A novel function of the receptor for advanced glycation end-products (RAGE) in association with tumorigenesis and tumor differentiation of HCC, Ann. Surg. Oncol. 2008, 15:923-933.
21. Cheng P., Dai W., Wang F., Lu J., Shen M., Chen K., Li J., Zhang Y., Wang C., Yang J., Zhu R., Zhang H., Zheng Y., Guo C.Y., Xu L. Ethyl pyruvate inhibits proliferation and induces apoptosis of hepatocellular carcinoma via regulation of the HMGB1-RAGE and AKT pathways. Biochem. Biophys. Res. Commun. 2014, 443:1162-1168.
22. Chen R.C., Yi P.P., Zhou R.R., Xiao M.F., Huang Z.B., Tang D.L., Huang Y., Fan X.G. The role of HMGB1-RAGE axis in migration and invasion of hepatocellular carcinoma cell lines. Mol. Cell. Biochem. 2014, 390:271-280.
23. Takino J., Yamagishi S., Takeuchi M. Glycer-AGEs-RAGE signaling enhances the angiogenic potential of hepatocellular carcinoma by upregulating VEGF expression. World J. Gastroenterol. 2012, 18:1781-1788.
24. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., Avila C., Kambham N., Bierhaus A., Nawroth P., Neurath M.F., Slattery T., Beach D., McClary J., Nagashima M., Morser J., Stern D., Schmidt A.M. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999, 97:889-901.
25. Dattilo B.M., Fritz G., Leclerc E., Kooi C.W., Heizmann C.W., Chazin W.J. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry 2007, 46:6957-6970.
26. Arumugam T., Simeone D.M., Schmidt A.M., Logsdon C.D. S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J. Biol. Chem. 2004, 279:5059-5065.
27. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr. Mol. Med. 2007, 7:711-724.
28. Ichikawa M., Williams R., Wang L., Vogl T., Srikrishna G. S100A8/A9 activate key genes and pathways in colon tumor progression. Mol. Cancer Res. 2011, 9:133-148.
29. Maletzki C., Bodammer P., Breitruck A., Kerkhoff C. S100 proteins as diagnostic and prognostic markers in colorectal and hepatocellular carcinoma. Hepat. Mon. 2012, 12:e7240.
30. Farahani E., Patra H.K., Jangamreddy J.R., Rashedi I., Kawalec M., Rao P.R., Batakis P., Wiechec E. Cell adhesion molecules and their relation to (cancer) cell stemness. Carcinogenesis 2014, 35:747-759.
31. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
32. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 2006, 8:1369-1375.
33. Srikrishna G. S100A8 and S100A9: new insights into their roles in malignancy. J. Innate Immun. 2012, 4:31-40.
34. Ghavami S., Chitayat S., Hashemi M., Eshraghi M., Chazin W.J., Halayko A.J., Kerkhoff C. S100A8/A9: a Janus-faced molecule in cancer therapy and tumorgenesis. Eur. J. Pharmacol. 2009, 625:73-83.
35. Moon A., Yong H.Y., Song J.I., Cukovic D., Salagrama S., Kaplan D., Putt D., Kim H., Dombkowski A., Kim H.R. Global gene expression profiling unveils S100A8/A9 as candidate markers in H-ras-mediated human breast epithelial cell invasion. Mol. Cancer Res. 2008, 6:1544-1553.
36. Kwon C.H., Moon H.J., Park H.J., Choi J.H., Park D.Y. S100A8 and S100A9 promotes invasion and migration through p38 mitogen-activated protein kinase-dependent NF-kappaB activation in gastric cancer cells. Mol. Cells 2013, 35:226-234.
37. Schmidt C.M., McKillop I.H., Cahill P.A., Sitzmann J.V. The role of cAMP-MAPK signalling in the regulation of human hepatocellular carcinoma growth in vitro. Eur. J. Gastroenterol. Hepatol. 1999, 11:1393-1399.
38. Huynh H., Nguyen T.T., Chow K.H., Tan P.H., Soo K.C., Tran E. Over-expression of the mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK in hepatocellular carcinoma: its role in tumor progression and apoptosis. BMC Gastroenterol. 2003, 3:19.
39. Nakagawa H., Maeda S. Molecular mechanisms of liver injury and hepatocarcinogenesis: focusing on the role of stress-activated MAPK. Pathol. Res. Int. 2012, 2012:172894.
40. Stern D., Yan S.D., Yan S.F., Schmidt A.M. Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings. Adv. Drug Deliv. Rev. 2002, 54:1615-1625.
41. Leclerc E., Fritz G., Weibel M., Heizmann C.W., Galichet A. S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J. Biol. Chem. 2007, 282:31317-31331.
42. Bopp C., Bierhaus A., Hofer S., Bouchon A., Nawroth P.P., Martin E., Weigand M.A. Bench-to-bedside review: the inflammation-perpetuating pattern-recognition receptor RAGE as a therapeutic target in sepsis. Crit. Care 2008, 12:201.
43. Li J., Schmidt A.M. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 1997, 272:16498-16506.
44. Jin Q., Chen H., Luo A., Ding F., Liu Z. S100A14 stimulates cell proliferation and induces cell apoptosis at different concentrations via receptor for advanced glycation end products (RAGE). PLoS One 2011, 6:e19375.
45. Tothova V., Gibadulinova A. S100P, a peculiar member of S100 family of calcium-binding proteins implicated in cancer. Acta Virol. 2013, 57:238-246.
46. Xu X., Chen H., Zhu X., Ma Y., Liu Q., Xue Y., Chu H., Wu W., Wang J., Zou H. S100A9 promotes human lung fibroblast cells activation through receptor for advanced glycation end-product-mediated extracellular-regulated kinase 1/2, mitogen-activated protein-kinase and nuclear factor-kappaB-dependent pathways. Clin. Exp. Immunol. 2013, 173:523-535.
47. Yeh C.H., Sturgis L., Haidacher J., Zhang X.N., Sherwood S.J., Bjercke R.J., Juhasz O., Crow M.T., Tilton R.G., Denner L. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 2001, 50:1495-1504.
48. Min L., He B., Hui L. Mitogen-activated protein kinases in hepatocellular carcinoma development. Semin. Cancer Biol. 2011, 21:10-20.
49. Gailhouste L., Ezan F., Bessard A., Fremin C., Rageul J., Langouet S., Baffet G. RNAi-mediated MEK1 knock-down prevents ERK1/2 activation and abolishes human hepatocarcinoma growth in vitro and in vivo. Int. J. Cancer 2010, 126:1367-1377.
50. Zhang K., Rui X., Yan X. Curcumin inhibits the proliferation and invasiveness of MHCC97-H cells via p38 signaling pathway. Drug Dev. Res. 2014, 75:463-468.
51. Park S.Y., Jeong K.J., Panupinthu N., Yu S., Lee J., Han J.W., Kim J.M., Lee J.S., Kang J., Park C.G., Mills G.B., Lee H.Y. Lysophosphatidic acid augments human hepatocellular carcinoma cell invasion through LPA1 receptor and MMP-9 expression. Oncogene 2011, 30:1351-1359.
52. Zhu B., Shi S., Ma Y.G., Fan F., Yao Z.Z. Lysophosphatidic acid enhances human hepatocellular carcinoma cell migration, invasion and adhesion through P38 MAPK pathway. Hepato-gastroenterology 2012, 59:785-789.
53. Gilet A., Zou F., Boumenir M., Frippiat J.P., Thornton S.N., Lacolley P., Ropars A. Aldosterone up-regulates MMP-9 and MMP-9/NGAL expression in human neutrophils through p38, ERK1/2 and PI3K pathways. Exp. Cell Res. 2014.
54. Wasik A.M., Grabarek J., Pantovic A., Cieslar-Pobuda A., Asgari H.R., Bundgaard-Nielsen C., Rafat M., Dixon I.M., Ghavami S., Los M.J. Reprogramming and carcinogenesis--parallels and distinctions. Int. Rev. Cell Mol. Biol. 2014, 308:167-203.
55. Wicha M.S., Liu S., Dontu G. Cancer stem cells: an old idea--a paradigm shift. Cancer Res. 2006, 66:1883-1890. 1895-1896.
56. Hombach-Klonisch S., Panigrahi S., Rashedi I., Seifert A., Alberti E., Pocar P., Kurpisz M., Schulze-Osthoff K., Mackiewicz A., Los M. Adult stem cells and their trans-differentiation potential--perspectives and therapeutic applications. J. Mol. Med. 2008, 86:1301-1314.
57. Lo J.F., Yu C.C., Chiou S.H., Huang C.Y., Jan C.I., Lin S.C., Liu C.J., Hu W.Y., Yu Y.H. The epithelial-mesenchymal transition mediator S100A4 maintains cancer-initiating cells in head and neck cancers. Cancer Res. 2011, 71:1912-1923.
58. Harris M.A., Yang H., Low B.E., Mukherjee J., Guha A., Bronson R.T., Shultz L.D., Israel M.A., Yun K. Cancer stem cells are enriched in the side population cells in a mouse model of glioma. Cancer Res. 2008, 68:10051-10059.
59. Leth-Larsen R., Terp M.G., Christensen A.G., Elias D., Kuhlwein T., Jensen O.N., Petersen O.W., Ditzel H.J. Functional heterogeneity within the CD44 high human breast cancer stem cell-like compartment reveals a gene signature predictive of distant metastasis. Mol. Med. 2012, 18:1109-1121.