Transcriptional regulation and functional implication of S100P in cancer

Amino Acids

Volumn 41, Issue 4, 2011, Pages 885-892

  Gibadulinova, Adriana ^a   Tothova, Veronika ^a   Pastorek, Jaromir ^a   Pastorekova, Silvia ^a,b  

^a INSTITUTE OF VIROLOGY   (Slovakia)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Calcium binding protein; Cancer; S100P; Transcriptional regulation

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ADVANCED GLYCATION END PRODUCT RECEPTOR; ANDROGEN RECEPTOR; BONE MORPHOGENETIC PROTEIN 4; CARBOPLATIN; CATHEPSIN D; CELECOXIB; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKERATIN; EPIRUBICIN; ETOPOSIDE; EZRIN; FLUOROURACIL; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; INTERLEUKIN 6; KRUPPEL LIKE FACTOR; OXALIPLATIN; PACLITAXEL; PROTEIN S 100; SHORT HAIRPIN RNA; SMAD PROTEIN; STAT PROTEIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER INVASION; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CELL PROTECTION; CELLULAR DISTRIBUTION; COLON CANCER; DNA METHYLATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR MECHANICS; ONCOGENE; OVARY CANCER; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; S100P GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION;

BINDING SITES; CALCIUM-BINDING PROTEINS; CYTOSKELETAL PROTEINS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; NEOPLASM PROTEINS; NEOPLASMS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, IMMUNOLOGIC; SMAD PROTEINS;

EID: 83255170627     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-010-0495-5     Document Type: Review

References (68)

1. Amler LC, Agus DB, LeDuc C, Sapinoso ML, Fox WD, Kern S, Lee D, Wang V, Leysens M, Higgins B, Martin J, Gerald W, Dracopoli N, Cordon-Cardo C, Scher HI, Hampton GM (2000) Dysregulated expression of androgen-responsive and nonresponsive genes in the androgen-independent prostate cancer xenograft model CWR22-R1. Cancer Res 60:6134-6141
2. Arumugam T, Simeone DM, Schmidt AM, Logsdon CD (2004) S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem 279:5059-5065
3. Arumugam T, Simeone DM, Van Golen K, Logsdon CD (2005) S100P promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res 11:5356-5364
4. Austermann J, Nazmi AR, Muller-Tidow C, Gerke V (2008) Characterization of the Ca2+-regulated ezrin-S100P interaction and its role in tumor cell migration. J Biol Chem 283:29331-29340
5. Averboukh L, Liang P, Kantoff PW, Pardee AB (1996) Regulation of S100P expression by androgen. Prostate 29:350-355
6. Bartling B, Rehbein G, Schmitt WD, Hofmann HS, Silber RE, Simm A (2007) S100A2-S100P expression profile and diagnosis of non-small cell lung carcinoma: impairment by advanced tumour stages and neoadjuvant chemotherapy. Eur J Cancer 43:1935-1943
7. Basu GD, Azorsa DO, Kiefer JA, Rojas AM, Tuzmen S, Barrett MT, Trent JM, Kallioniemi O, Mousses S (2008) Functional evidence implicating S100P in prostate cancer progression. Int J Cancer 123:330-339
8. Becker T, Gerke V, Kube E, Weber K (1992) S100P, a novel Ca(2?)- binding protein from human placenta. cDNA cloning, recombinant protein expression and Ca2+ binding properties. Eur J Biochem 207:541-547
9. Bertram J, Palfner K, Hiddemann W, Kneba M (1998) Elevated expression of S100P, CAPL and MAGE 3 in doxorubicinresistant cell lines: comparison of mRNA differential display reverse transcription-polymerase chain reaction and subtractive suppressive hybridization for the analysis of differential gene expression. Anticancer Drugs 9:311-317
10. Black AR, Black JD, Azizkhan-Clifford J (2001) Sp1 and kruppellike factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 188:143-160
11. Bray JD, Jelinsky S, Ghatge R, Bray JA, Tunkey C, Saraf K, Jacobsen BM, Richer JK, Brown EL, Winneker RC, Horwitz KB, Lyttle CR (2005) Quantitative analysis of gene regulation by seven clinically relevant progestins suggests a highly similar mechanism of action through progesterone receptors in T47D breast cancer cells. J Steroid Biochem Mol Biol 97:328-341
12. Bulk E, Hascher A, Liersch R, Mesters RM, Diederichs S, Sargin B, Gerke V, Hotfilder M, Vormoor J, Berdel WE, Serve H, Muller- Tidow C (2008) Adjuvant therapy with small hairpin RNA interference prevents non-small cell lung cancer metastasis development in mice. Cancer Res 68:1896-1904
13. Crnogorac-Jurcevic T, Missiaglia E, Blaveri E, Gangeswaran R, Jones M, Terris B, Costello E, Neoptolemos JP, Lemoine NR (2003) Molecular alterations in pancreatic carcinoma: expression profiling shows that dysregulated expression of S100 genes is highly prevalent. J Pathol 201:63-74
14. Deng H, Shi J, Wilkerson M, Meschter S, Dupree W, Lin F (2008) Usefulness of S100P in diagnosis of adenocarcinoma of pancreas on fine-needle aspiration biopsy specimens. Am J Clin Pathol 129:81-88
15. Diederichs S, Bulk E, Steffen B, Ji P, Tickenbrock L, Lang K, Zanker KS, Metzger R, Schneider PM, Gerke V, Thomas M, Berdel WE, Serve H, Muller-Tidow C (2004) S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage non-small cell lung cancer. Cancer Res 64:5564-5569
16. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60:540-551
17. Dowen SE, Crnogorac-Jurcevic T, Gangeswaran R, Hansen M, Eloranta JJ, Bhakta V, Brentnall TA, Luttges J, Kloppel G, Lemoine NR (2005) Expression of S100P and its novel binding partner S100PBPR in early pancreatic cancer. Am J Pathol 166:81-92
18. Filipek A, Jastrzebska B, Nowotny M, Kuznicki J (2002) CacyBP/ SIP, a calcyclin and Siah-1-interacting protein, binds EF-hand proteins of the S100 family. J Biol Chem 277:28848-28852
19. Fuentes MK, Nigavekar SS, Arumugam T, Logsdon CD, Schmidt AM, Park JC, Huang EH (2007) RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis Colon Rectum 50:1230-1240
20. Fukushima N, Sato N, Prasad N, Leach SD, Hruban RH, Goggins M (2004) Characterization of gene expression in mucinous cystic neoplasms of the pancreas using oligonucleotide microarrays. Oncogene 23:9042-9051
21. Gibadulinova A, Barathova M, Kopacek J, Hulikova A, Pastorekova S, Kettmann R, Pastorek J (2005) Expression of S100P protein correlates with and contributes to the tumorigenic capacity of HeLa cervical carcinoma cells. Oncol Rep 14:575-582
22. Gibadulinova A, Oveckova I, Parkkila S, Pastorekova S, Pastorek J (2008) Key promoter elements involved in transcriptional activation of the cancer-related gene coding for S100P calcium- binding protein. Oncol Rep 20:391-396
23. Gribenko AV, Hopper JE, Makhatadze GI (2001) Molecular characterization and tissue distribution of a novel member of the S100 family of EF-hand proteins. Biochemistry 40:15538-15548
24. Guerreiro Da Silva ID, Hu YF, Russo IH, Ao X, Salicioni AM, Yang X, Russo J (2000) S100P calcium-binding protein overexpression is associated with immortalization of human breast epithelial cells in vitro and early stages of breast cancer development in vivo. Int J Oncol 16:231-240
25. Hamada S, Satoh K, Hirota M, Fujibuchi W, Kanno A, Umino J, Ito H, Satoh A, Kikuta K, Kume K, Masamune A, Shimosegawa T (2009) Expression of the calcium-binding protein S100P is regulated by bone morphogenetic protein in pancreatic duct epithelial cell lines. Cancer Sci 100:103-110
26. Hammacher A, Thompson EW, Williams ED (2005) Interleukin-6 is a potent inducer of S100P, which is up-regulated in androgenrefractory and metastatic prostate cancer. Int J Biochem Cell Biol 37:442-450
27. He Z, Gao J, Wang Q, Liu M, Li Y, Li X, Tang H, Zheng J (2008) S100P contributes to chemosensitivity of human ovarian cancer cell line OVCAR3. Oncol Rep 20:325-332
28. Heizmann CW, Cox JA (1998) New perspectives on S100 proteins: a multi-functional Ca(2?)-, Zn(2?)- and Cu(2?)-binding protein family. Biometals 11:383-397
29. Heizmann CW, Fritz G, Schafer BW (2002) S100 proteins: structure, functions and pathology. Front Biosci 7:d1356-d1368
30. 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
31. Hsieh HL, Schafer BW, Weigle B, Heizmann CW (2004) S100 protein translocation in response to extracellular S100 is mediated by receptor for advanced glycation endproducts in human endothelial cells. Biochem Biophys Res Commun 316:949-959
32. Jakubickova L, Barathova M, Pastorekova S, Pastorek J, Gibadulinova A (2005) Expression of S100P gene in cervical carcinoma cells is independent of E7 human papillomavirus oncogene. Acta Virol 49:133-137
33. Jiang F, Shults K, Flye L, Hashimoto Y, Van Der Meer R, Xie J, Kravtsov V, Price J, Head DR, Briggs RC (2005) S100P is selectively upregulated in tumor cell lines challenged with DNA cross-linking agents. Leuk Res 29:1181-1190
34. Kassel O, Herrlich P (2007) Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 275:13-29
35. Kino T, Manoli I, Kelkar S, Wang Y, Su YA, Chrousos GP (2009) Glucocorticoid receptor (GR) beta has intrinsic, GRalphaindependent transcriptional activity. Biochem Biophys Res Commun 381:671-675
36. Koltzscher M, Gerke V (2000) Identification of hydrophobic amino acid residues involved in the formation of S100P homodimers in vivo. Biochemistry 39:9533-9539
37. Koltzscher M, Neumann C, Konig S, Gerke V (2003) Ca2+- dependent binding and activation of dormant ezrin by dimeric S100P. Mol Biol Cell 14:2372-2384
38. Logsdon CD, Simeone DM, Binkley C, Arumugam T, Greenson JK, Giordano TJ, Misek DE, Kuick R, Hanash S (2003) Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res 63:2649-2657
39. Mandinova A, Atar D, Schafer BW, Spiess M, Aebi U, Heizmann CW (1998) Distinct subcellular localization of calcium binding S100 proteins in human smooth muscle cells and their relocation in response to rises in intracellular calcium. J Cell Sci 111(Pt 14):2043-2054
40. Marenholz I, Heizmann CW, Fritz G (2004) 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
41. Marenholz I, Lovering RC, Heizmann CW (2006) An update of the S100 nomenclature. Biochim Biophys Acta 1763:1282-1283
42. Matsuzawa SI, Reed JC (2001) Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol Cell 7:915-926
43. Mattern J, Buchler MW, Herr I (2007) Cell cycle arrest by glucocorticoids may protect normal tissue and solid tumors from cancer therapy. Cancer Biol Ther 6:1345-1354
44. McCabe MT, Brandes JC, Vertino PM (2009) Cancer DNA methylation: molecular mechanisms and clinical implications. Clin Cancer Res 15:3927-3937
45. Missiaglia E, Blaveri E, Terris B, Wang YH, Costello E, Neoptolemos JP, Crnogorac-Jurcevic T, Lemoine NR (2004) Analysis of gene expression in cancer cell lines identifies candidate markers for pancreatic tumorigenesis and metastasis. Int J Cancer 112:100-112
46. Mousses S, Wagner U, Chen Y, Kim JW, Bubendorf L, Bittner M, Pretlow T, Elkahloun AG, Trepel JB, Kallioniemi OP (2001) Failure of hormone therapy in prostate cancer involves systematic restoration of androgen responsive genes and activation of rapamycin sensitive signaling. Oncogene 20:6718-6723
47. Mousses S, Bubendorf L, Wagner U, Hostetter G, Kononen J, Cornelison R, Goldberger N, Elkahloun AG, Willi N, Koivisto P, Ferhle W, Raffeld M, Sauter G, Kallioniemi OP (2002) Clinical validation of candidate genes associated with prostate cancer progression in the CWR22 model system using tissue microarrays. Cancer Res 62:1256-1260
48. Mueller A, Bachi T, Hochli M, Schafer BW, Heizmann CW (1999) Subcellular distribution of S100 proteins in tumor cells and their relocation in response to calcium activation. Histochem Cell Biol 111:453-459
49. Namba T, Homan T, Nishimura T, Mima S, Hoshino T, Mizushima T (2009) Up-regulation of S100P expression by non-steroidal antiinflammatory drugs and its role in anti-tumorigenic effects. J Biol Chem 284:4158-4167
50. Ohuchida K, Mizumoto K, Egami T, Yamaguchi H, Fujii K, Konomi H, Nagai E, Yamaguchi K, Tsuneyoshi M, Tanaka M (2006) S100P is an early developmental marker of pancreatic carcinogenesis. Clin Cancer Res 12:5411-5416
51. Parkkila S, Pan PW, Ward A, Gibadulinova A, Oveckova I, Pastorekova S, Pastorek J, Martinez AR, Helin HO, Isola J (2008) The calcium-binding protein S100P in normal and malignant human tissues. BMC Clin Pathol 8:2.
52. Rehbein G, Simm A, Hofmann HS, Silber RE, Bartling B (2008) Molecular regulation of S100P in human lung adenocarcinomas. Int J Mol Med 22:69-77
53. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006) Calcium-dependent and -independent interactions of the S100 protein family. Biochem J 396:201-214
54. Sato N, Hitomi J (2002) S100P expression in human esophageal epithelial cells: human esophageal epithelial cells sequentially produce different S100 proteins in the process of differentiation. Anat Rec 267:60-69
55. Sato N, Fukushima N, Matsubayashi H, Goggins M (2004) Identification of maspin and S100P as novel hypomethylation targets in pancreatic cancer using global gene expression profiling. Oncogene 23:1531-1538
56. Schoneveld OJ, Gaemers IC, Lamers WH (2004) Mechanisms of glucocorticoid signalling. Biochim Biophys Acta 1680:114-128
57. Schor AP, Carvalho FM, Kemp C, Silva ID, Russo J (2006) S100P calcium-binding protein expression is associated with high-risk proliferative lesions of the breast. Oncol Rep 15:3-6
58. Song J, Shih IeM, Chan DW, Zhang Z (2009): Suppression of annexin A11 in ovarian cancer: implications in chemoresistance. Neoplasia 11:605-614, 1 p following 614
59. Surowiak P, Maciejczyk A, Materna V, Drag-Zalesinska M, Wojnar A, Pudelko M, Kedzia W, Spaczynski M, Dietel M, Zabel M, Lage H (2007) Unfavourable prognostic significance of S100P expression in ovarian cancers. Histopathology 51:125-128
60. Terris B, Blaveri E, Crnogorac-Jurcevic T, Jones M, Missiaglia E, Ruszniewski P, Sauvanet A, Lemoine NR (2002) Characterization of gene expression profiles in intraductal papillary-mucinous tumors of the pancreas. Am J Pathol 160:1745-1754
61. Tutar Y (2006) Dimerization and ion binding properties of S100P protein. Protein Pept Lett 13:301-306
62. Wang G, Zhang S, Fernig DG, Spiller D, Martin-Fernandez M, Zhang H, Ding Y, Rao Z, Rudland PS, Barraclough R (2004) Heterodimeric interaction and interfaces of S100A1 and S100P. Biochem J 382:375-383
63. Wang G, Platt-Higgins A, Carroll J, de Silva Rudland S, Winstanley J, Barraclough R, Rudland PS (2006) Induction of metastasis by S100P in a rat mammary model and its association with poor survival of breast cancer patients. Cancer Res 66:1199-1207
64. Wang Q, Williamson M, Bott S, Brookman-Amissah N, Freeman A, Nariculam J, Hubank MJ, Ahmed A, Masters JR (2007) Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer. Oncogene 26:6560-6565
65. Wang Q, He Z, Gao J, Hu S, Huang M, Liu M, Zheng J, Tang H (2008) S100P sensitizes ovarian cancer cells to carboplatin and paclitaxel in vitro. Cancer Lett 272:277-284
66. Whiteman HJ, Weeks ME, Dowen SE, Barry S, Timms JF, Lemoine NR, Crnogorac-Jurcevic T (2007) The role of S100P in the invasion of pancreatic cancer cells is mediated through cytoskeletal changes and regulation of cathepsin D. Cancer Res 67:8633-8642
67. Zhang H, Wang Z, Ding Y, Wang G, Wang X, Gao F, Tang H, Barraclough R, Rudland PS, Rao Z (2002) Purification, crystallization and preliminary X-ray diffraction studies of a Ca2+- binding protein, human S100P. Acta Crystallogr D Biol Crystallogr 58:694-696
68. Zhang H, Wang G, Ding Y, Wang Z, Barraclough R, Rudland PS, Fernig DG, Rao Z (2003) The crystal structure at 2A resolution of the Ca2+-binding protein S100P. J Mol Biol 325:785-794