S100A2 in cancerogenesis: A friend or a foe?

Amino Acids

Volumn 41, Issue 4, 2011, Pages 849-861

  Wolf, Susann ^a   Haase Kohn, Cathleen ^a   Pietzsch, Jens ^a  

^a INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

Author keywords

EF hand; Keywords Calcium binding protein; P53 Protein family; Receptor for advanced glycation endproducts (RAGE); Tumor promotor; Tumor suppressor

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; PROTEIN S100A2; UNCLASSIFIED DRUG; ZINC ION;

CARCINOGENESIS; CELL NUCLEUS; CELL TRANSFORMATION; DOWN REGULATION; GENE STRUCTURE; HUMAN; METASTASIS; MOLECULAR PATHOLOGY; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; TUMOR; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; CHEMOTACTIC FACTORS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; S100 PROTEINS; UP-REGULATION;

EID: 83255187592     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-010-0623-2     Document Type: Review

References (91)

1. Almadori G et al (2009) Diminished expression of S100A2, a putative tumour suppressor, is an independent predictive factor of neck node relapse in laryngeal squamous cell carcinoma. J Otolaryngol Head Neck Surg 38:16-22
2. Andersen LB, Xia L, Stoll S, Zhao X, Elder JT (1996) Lineagespecific CaN19 expression in human skin: lack of expression in normal melanocytes. J Dermatol Sci 12:69-72
3. 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
4. Biankin AV et al (2009) Expression of S100A2 calcium-binding protein predicts response to pancreatectomy for pancreatic cancer. Gastroenterology 137:558-568, 568 e551-511
5. 2+ binding S100 proteins in normal human skin and melanocytic lesions. Br J Dermatol 137:39-43
6. Botelho HM, Koch M, Fritz G, Gomes CM (2009) Metal ions modulate the folding and stability of the tumor suppressor protein S100A2. FEBS J 276:1776-1786
7. Bulk E et al (2009) S100A2 induces metastasis in non-small cell lung cancer. Clin Cancer Res 15:22-29
8. Cao LY, Yin Y, Li H, Jiang Y, Zhang HF (2009) Expression and clinical significance of S100A2 and p63 in esophageal carcinoma. World J Gastroenterol 15:4183-4188
9. Chen Z, Zhang K, Zhang X, Yuan XH, Yuan Z, Jin L, Xiong M (2003) Comparison of gene expression between metastatic derivatives and their poorly metastatic parental cells implicates crucial tumor-environment interaction in metastasis of head and neck squamous cell carcinoma. Clin Exp Metastasis 20:335-342
10. Craig RW, Jabs EW, Zhou P, Kozopas KM, Hawkins AL, Rochelle JM, Seldin MF, Griffin CA (1994) Human and mouse chromosomal mapping of the myeloid cell leukemia-1 gene: MCL1 maps to human chromosome 1q21, a region that is frequently altered in preneoplastic and neoplastic disease. Genomics 23:457-463
11. Deshpande R, Woods TL, Fu J, Zhang T, Stoll SW, Elder JT (2000) Biochemical characterization of S100A2 in human keratinocytes: subcellular localization, dimerization, and oxidative crosslinking. J Invest Dermatol 115:477-485
12. Diederichs S et al (2004) S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage nonsmall cell lung cancer. Cancer Res 64:5564-5569
13. Donato R (2003) Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60:540-551
14. Eckert RL, Broome AM, Ruse M, Robinson N, Ryan D, Lee K (2004) S100 proteins in the epidermis. J Invest Dermatol 123:23-33
15. Elder JT, Zhao X (2002) Evidence for local control of gene expression in the epidermal differentiation complex. Exp Dermatol 11:406-412
16. El-Rifai W, Moskaluk CA, Abdrabbo MK, Harper J, Yoshida C, Riggins GJ, Frierson HF Jr, Powell SM (2002) Gastric cancers overexpress S100A calcium-binding proteins. Cancer Res 62:6823-6826
17. Engelkamp D, Schafer BW, Mattei MG, Erne P, Heizmann CW (1993) Six S100 genes are clustered on human chromosome 1q21: identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E. Proc Natl Acad Sci USA 90:6547-6551
18. Feng G, Xu X, Youssef EM, Lotan R (2001) Diminished expression of S100A2, a putative tumor suppressor, at early stage of human lung carcinogenesis. Cancer Res 61:7999-8004
19. Fernandez-Fernandez MR, Rutherford TJ, Fersht AR (2008) Members of the S100 family bind p53 in two distinct ways. Protein Sci 17:1663-1670
20. Foser S, Redwanz I, Ebeling M, Heizmann CW, Certa U (2006) Interferon-alpha and transforming growth factor-beta co-induce growth inhibition of human tumor cells. Cell Mol Life Sci 63:2387-2396
21. 2+ to human nuclear S100A2 and mutant proteins. J Biol Chem 273:18826-18834
22. 2+-dependent interaction of S100A2 with muscle and nonmuscle tropomyosins. J Cell Sci 110(Pt 5):611-621
23. Glenney JR Jr, Kindy MS, Zokas L (1989) Isolation of a new member of the S100 protein family: amino acid sequence, tissue, and subcellular distribution. J Cell Biol 108:569-578
24. Gollob JA, Sciambi CJ (2007) Decitabine up-regulates S100A2 expression and synergizes with IFN-gamma to kill uveal melanoma cells. Clin Cancer Res 13:5219-5225
25. Gupta S, Hussain T, MacLennan GT, Fu P, Patel J, Mukhtar H (2003) Differential expression of S100A2 and S100A4 during progression of human prostate adenocarcinoma. J Clin Oncol 21:106-112
26. Heighway J et al (2002) Expression profiling of primary non-small cell lung cancer for target identification. Oncogene 21:7749-7763
27. +)-binding protein family. Biometals 11:383-397
28. Hibi K, Fujitake S, Takase T, Kodera Y, Ito K, Akiyama S, Shirane M, Nakao A (2003) Identification of S100A2 as a target of the DeltaNp63 oncogenic pathway. Clin Cancer Res 9:4282-4285
29. Hough CD, Cho KR, Zonderman AB, Schwartz DR, Morin PJ (2001) Coordinately up-regulated genes in ovarian cancer. Cancer Res 61:3869-3876
30. +)-binding S-100 proteins S-100A1, S-100A2, S-100A4, S-100A6 and S-100B in salivary gland tumors. J Oral Pathol Med 25:547-555
31. Ilg EC, Schafer BW, Heizmann CW (1996) Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68:325-332
32. Imazawa M, Hibi K, Fujitake S, Kodera Y, Ito K, Akiyama S, Nakao A (2005) S100A2 overexpression is frequently observed in esophageal squamous cell carcinoma. Anticancer Res 25:1247-1250
33. Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, Kobayashi K, Matsuzuka F, Kakudo K, Kuma K, Miyauchi A (2005) Expression of S100A2 and S100A6 in thyroid carcinomas. Histopathology 46:569-575
34. Jeronimo C, Henrique R, Hoque MO, Mambo E, Ribeiro FR, Varzim G, Oliveira J, Teixeira MR, Lopes C, Sidransky D (2004) A quantitative promoter methylation profile of prostate cancer. Clin Cancer Res 10:8472-8478
35. Ji J, Zhao L, Wang X, Zhou C, Ding F, Su L, Zhang C, Mao X, Wu M, Liu Z (2004) Differential expression of S100 gene family in human esophageal squamous cell carcinoma. J Cancer Res Clin Oncol 130:480-486
36. Kirschner RD, Sanger K, Muller GA, Engeland K (2008) Transcriptional activation of the tumor suppressor and differentiation gene S100A2 by a novel p63-binding site. Nucleic Acids Res 36:2969-2980
37. Klopper JP, Sharma V, Bissonnette R, Haugen BR (2010) Combination PPARgamma and RXR agonist treatment in melanoma cells: functional importance of S100A2. PPAR Res 2010:729876
38. Koch M, Diez J, Fritz G (2006) Purification and crystallization of the human EF-hand tumour suppressor protein S100A2. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:1120-1123
39. Koch M, Bhattacharya S, Kehl T, Gimona M, Vasak M, Chazin W, Heizmann CW, Kroneck PM, Fritz G (2007) Implications on zinc binding to S100A2. Biochim Biophys Acta 1773:457-470
40. 2+-free S100A2 at 1.6-A resolution. J Mol Biol 378:933-942
41. Komada T, Araki R, Nakatani K, Yada I, Naka M, Tanaka T (1996) Novel specific chemtactic receptor for S100L protein on guinea pig eosinophils. Biochem Biophys Res Commun 220:871-874
42. Kyriazanos ID, Tachibana M, Dhar DK, Shibakita M, Ono T, Kohno H, Nagasue N (2002) Expression and prognostic significance of S100A2 protein in squamous cell carcinoma of the esophagus. Oncol Rep 9:503-510
43. Lapi E, Iovino A, Fontemaggi G, Soliera AR, Iacovelli S, Sacchi A, Rechavi G, Givol D, Blandino G, Strano S (2006) S100A2 gene is a direct transcriptional target of p53 homologues during keratinocyte differentiation. Oncogene 25:3628-3637
44. +) binding protein S100A2 in laryngeal squamous-cell carcinoma. Int J Cancer 89:345-349
45. Leclerc E, Fritz G, Vetter SW, Heizmann CW (2008) Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 1793:993-1007
46. Lee SW, Tomasetto C, Sager R (1991) Positive selection of candidate tumor-suppressor genes by subtractive hybridization. Proc Natl Acad Sci USA 88:2825-2829
47. Lee SW, Tomasetto C, Swisshelm K, Keyomarsi K, Sager R (1992) Down-regulation of a member of the S100 gene family in mammary carcinoma cells and reexpression by azadeoxycytidine treatment. Proc Natl Acad Sci USA 89:2504-2508
48. Lee OJ, Hong SM, Razvi MH, Peng D, Powell SM, Smoklin M, Moskaluk CA, El-Rifai W (2006) Expression of calcium-binding proteins S100A2 and S100A4 in Barrett's adenocarcinomas. Neoplasia 8:843-850
49. Li Y, Gudjonsson JE, Woods TL, Zhang T, Johnston A, Stoll SW, Elder JT (2009) Transgenic expression of S100A2 in hairless mouse skin enhances Cxcl13 mRNA in response to solarsimulated radiation. Arch Dermatol Res 301:205-217
50. Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R (2000) Expression of calcium-binding protein S100A2 in breast lesions. Br J Cancer 83:1473-1479
51. Liu J, Li X, Dong GL, Zhang HW, Chen DL, Du JJ, Zheng JY, Li JP, Wang WZ (2008) In silico analysis and verification of S100 gene expression in gastric cancer. BMC Cancer 8:261
52. Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O (1997) Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int J Cancer 74:464-469
53. 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
54. 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
55. Matsubara D et al (2005) Differential expression of S100A2 and S100A4 in lung adenocarcinomas: clinicopathological significance, relationship to p53 and identification of their target genes. Cancer Sci 96:844-857
56. Matsumoto K, Irie A, Satoh T, Ishii J, Iwabuchi K, Iwamura M, Egawa S, Baba S (2007) Expression of S100A2 and S100A4 predicts for disease progression and patient survival in bladder cancer. Urology 70:602-607
57. 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
58. Mueller A, Schafer BW, Ferrari S, Weibel M, Makek M, Hochli M, Heizmann CW (2005) The calcium-binding protein S100A2 interacts with p53 and modulates its transcriptional activity. J Biol Chem 280:29186-29193
59. Nagy N et al (2001) S100A2, a putative tumor suppressor gene, regulates in vitro squamous cell carcinoma migration. Lab Invest 81:599-612
60. 2+- binding S100A2 protein is differentially expressed in epithelial tissue of glandular or squamous origin. Histol Histopathol 17:123-130
61. Nonaka D, Chiriboga L, Rubin BP (2008) Differential expression of S100 protein subtypes in malignant melanoma, and benign and malignant peripheral nerve sheath tumors. J Cutan Pathol 35:1014-1019
62. Ohuchida K, Mizumoto K, Ishikawa N, Fujii K, Konomi H, Nagai E, Yamaguchi K, Tsuneyoshi M, Tanaka M (2005) 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
63. Ohuchida K et al (2007) Over-expression of S100A2 in pancreatic cancer correlates with progression and poor prognosis. J Pathol 213:275-282
64. +)-binding proteins of the S100 family in malignant human breast-cancer cell lines and biopsy samples. Int J Cancer 57:684-690
65. +)-bound S100A2 from NMR and homology modeling. Biochem Biophys Res Commun 288:462-467
66. Ravasi T, Hsu K, Goyette J, Schroder K, Yang Z, Rahimi F, Miranda LP, Alewood PF, Hume DA, Geczy C (2004) Probing the S100 protein family through genomic and functional analysis. Genomics 84:10-22
67. Rehman I, Cross SS, Catto JW, Leiblich A, Mukherjee A, Azzouzi AR, Leung HY, Hamdy FC (2005) Promoter hyper-methylation of calcium binding proteins S100A6 and S100A2 in human prostate cancer. Prostate 65:322-330
68. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006) Calcium- dependent and -independent interactions of the S100 protein family. Biochem J 396:201-214
69. Shimamoto S, Takata M, Tokuda M, Oohira F, Tokumitsu H, Kobayashi R (2008) Interactions of S100A2 and S100A6 with the tetratricopeptide repeat proteins, Hsp90/Hsp70-organizing protein and kinesin light chain. J Biol Chem 283:28246-28258
70. +)- binding S100 proteins in epithelial tumours of the skin. Virchows Arch 432:53-59
71. Smith SL, Gugger M, Hoban P, Ratschiller D, Watson SG, Field JK, Betticher DC, Heighway J (2004) S100A2 is strongly expressed in airway basal cells, preneoplastic bronchial lesions and primary non-small cell lung carcinomas. Br J Cancer 91:1515-1524
72. Stoll SW, Zhao X, Elder JT (1998) EGF stimulates transcription of CaN19 (S100A2) in HaCaT keratinocytes. J Invest Dermatol 111:1092-1097
73. Stoll SW, Chia NV, Nair RP, Woods TL, Stuart P, Henseler T, Jenisch S, Christophers E, Voorhees JJ, Elder JT (2001) S100A2 coding sequence polymorphism: characterization and lack of association with psoriasis. Clin Exp Dermatol 26:79-83
74. Stradal TB, Troxler H, Heizmann CW, Gimona M (2000) Mapping the zinc ligands of S100A2 by site-directed mutagenesis. J Biol Chem 275:13219-13227
75. Strazisar M, Rott T, Glavac D (2009a) Frequent polymorphic variations but rare tumour specific mutations of the S100A2 on 1q21 in non-small cell lung cancer. Lung Cancer 63:354-359
76. Strazisar M, Mlakar V, Glavac D (2009b) The expression of COX-2, hTERT, MDM2, LATS2 and S100A2 in different types of nonsmall cell lung cancer (NSCLC). Cell Mol Biol Lett 14:442-456
77. Suzuki F, Oridate N, Homma A, Nakamaru Y, Nagahashi T, Yagi K, Yamaguchi S, Furuta Y, Fukuda S (2005) S100A2 expression as a predictive marker for late cervical metastasis in stage I and II invasive squamous cell carcinoma of the oral cavity. Oncol Rep 14:1493-1498
78. Tan M, Heizmann CW, Guan K, Schafer BW, Sun Y (1999) Transcriptional activation of the human S100A2 promoter by wild-type p53. FEBS Lett 445:265-268
79. Tsai ST, Jin YT, Tsai WC, Wang ST, Lin YC, Chang MT, Wu LW (2005) S100A2, a potential marker for early recurrence in earlystage oral cancer. Oral Oncol 41:349-357
80. Tsai WC, Tsai ST, Jin YT, Wu LW (2006) Cyclooxygenase-2 is involved in S100A2-mediated tumor suppression in squamous cell carcinoma. Mol Cancer Res 4:539-547
81. van Dieck J, Fernandez-Fernandez MR, Veprintsev DB, Fersht AR (2009a) Modulation of the oligomerization state of p53 by differential binding of proteins of the S100family to p53 monomers and tetramers. J Biol Chem 284:13804-13811
82. van Dieck J, Teufel DP, Jaulent AM, Fernandez-Fernandez MR, Rutherford TJ, Wyslouch-Cieszynska A, Fersht AR (2009b) Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53. J Mol Biol 394:922-930
83. van Dieck J, Brandt T, Teufel DP, Veprintsev DB, Joerger AC, Fersht AR (2010) Molecular basis of S100 proteins interacting with the p53 homologs p63 and p73. Oncogene 29:2024-2035
84. Villaret DB, Wang T, Dillon D, Xu J, Sivam D, Cheever MA, Reed SG (2000) Identification of genes overexpressed in head and neck squamous cell carcinoma using a combination of complementary DNA subtraction and microarray analysis. Laryngoscope 110:374-381
85. Wang H, Zhang Z, Li R, Ang KK, Zhang H, Caraway NP, Katz RL, Jiang F (2005) Overexpression of S100A2 protein as a prognostic marker for patients with stage I non small cell lung cancer. Int J Cancer 116:285-290
86. Wicki R, Franz C, Scholl FA, Heizmann CW, Schafer BW (1997) Repression of the candidate tumor suppressor gene S100A2 in breast cancer is mediated by site-specific hypermethylation. Cell Calcium 22:243-254
87. Xia L, Stoll SW, Liebert M, Ethier SP, Carey T, Esclamado R, Carroll W, Johnson TM, Elder JT (1997) CaN19 expression in benign and malignant hyperplasias of the skin and oral mucosa: evidence for a role in regenerative differentiation. Cancer Res 57:3055-3062
88. Yang A, Kaghad M, Caput D, McKeon F (2002) On the shoulders of giants: p63, p73 and the rise of p53. Trends Genet 18:90-95
89. Zech VF, Dlaska M, Tzankov A, Hilbe W (2006) Prognostic and diagnostic relevance of hnRNP A2/B1, hnRNP B1 and S100 A2 in non-small cell lung cancer. Cancer Detect Prev 30:395-402
90. Zhang T, Woods TL, Elder JT (2002) Differential responses of S100A2 to oxidative stress and increased intracellular calcium in normal, immortalized, and malignant human keratinocytes. J Invest Dermatol 119:1196-1201
91. Zhang X, Hunt JL, Shin DM, Chen ZG (2007) Down-regulation of S100A2 in lymph node metastases of head and neck cancer. Head Neck 29:236-243