Increased cytoplasmic S100A6 expression is associated with pulmonary adenocarcinoma progression

Pathology International

Volumn 59, Issue 9, 2009, Pages 623-630

  Ishii, Aya ^a   Suzuki, Meguri ^a   Satomi, Kaishi ^a   Kobayashi, Hiromi ^a   Sakashita, Shingo ^a   Kano, Junko ^a   Pei, Yihua ^a   Minami, Yuko ^a   Ishikawa, Shigemi ^a   Noguchi, Masayuki ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

BAC; Immunohistochemistry; Lung adenocarcinoma; S100A6; Western blotting

Indexed keywords

CALCYCLIN; TUMOR MARKER;

ADULT; ADVANCED CANCER; AGED; ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER TISSUE; CARCINOMA CELL; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG ALVEOLUS CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ADENOCARCINOMA, BRONCHIOLO-ALVEOLAR; ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; CELL COUNT; CELL CYCLE PROTEINS; CELL NUCLEUS; CYTOPLASM; DISEASE PROGRESSION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MALE; MIDDLE AGED; NEOPLASM STAGING; S100 PROTEINS; TUMOR MARKERS, BIOLOGICAL;

EID: 68949086327     PISSN: 13205463     EISSN: 14401827     Source Type: Journal    
DOI: 10.1111/j.1440-1827.2009.02417.x     Document Type: Article

References (45)

1. Greenlee RT, Hill-Harmon MB, Murray T, Thun M. Cancer statistics, 2001. CA Cancer J Clin 2001 51 : 15 36.
2. Sone S, Takashima S, Li F et al. Mass screening for lung cancer with mobile spiral computed tomography scanner. Lancet 1998 351 : 1242 5.
3. Noguchi M, Morikawa A, Kawasaki M et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer 1995 75 : 2844 52.
4. Suzuki K, Yokose T, Yoshida J et al. Prognostic significance of the size of central fibrosis in peripheral adenocarcinoma of the lung. Ann Thorac Surg 2000 69 : 893 7.
5. Sakurai H, Maeshima A, Watanabe S et al. Grade of stromal invasion in small adenocarcinoma of the lung: Histopathological minimal invasion and prognosis. Am J Surg Pathol 2004 28 : 198 206.
6. Ishiyama T, Kano J, Anami Y et al. OCIA domain containing 2 is highly expressed in adenocarcinoma mixed subtype with bronchioloalveolar carcinoma component and is associated with better prognosis. Cancer Sci 2007 98 : 50 57.
7. Ridinger K, Ilg EC, Niggli FK, Heizmann CW, Schafer BW. Clustered organization of S100 genes in human and mouse. Biochim Biophys Acta 1998 1448 : 254 63.
8. Bartling B, Rehbein G, Schmitt WD, Hofmann HS, Silber RE, Simm A. S100A2-S100P expression profile and diagnosis of non-small cell lung carcinoma: Impairment by advanced tumour stages and neoadjuvant chemotherapy. Eur J Cancer 2007 43 : 1935 43.
9. Chen XL, Zhang WG, Chen XY, Sun ZM, Liu SH Correlations of S100A4 protein expression to invasion and metastasis of non-small cell lung cancer Ai Zheng 2006 25 : 1134 7.
10. Zhang H, Wang Y, Chen Y et al. Identification and validation of S100A7 associated with lung squamous cell carcinoma metastasis to brain. Lung Cancer 2007 57 : 37 45.
11. Arai K, Teratani T, Nozawa R, Yamada T. Immunohistochemical investigation of S100A9 expression in pulmonary adenocarcinoma: S100A9 expression is associated with tumor differentiation. Oncol Rep 2001 8 : 591 6.
12. Calabretta B, Kaczmarek L, Mars W et al. Cell-cycle-specific genes differentially expressed in human leukemias. Proc Natl Acad Sci USA 1985 82 : 4463 7.
13. Kuznicki J, Filipek A. Purification and properties of a novel Ca2+-binding protein (10.5 kDa) from Ehrlich-ascites-tumour cells. Biochem J 1987 247 : 663 7.
14. Otterbein LR, Kordowska J, Witte-Hoffmann C, Wang CL, Dominguez R. Crystal structures of S100A6 in the Ca(2+)-free and Ca(2+)-bound states: The calcium sensor mechanism of S100 proteins revealed at atomic resolution. Structure 2002 10 : 557 67.
15. Calabretta B, Battini R, Kaczmarek L, de Riel JK, Baserga R. Molecular cloning of the cDNA for a growth factor-inducible gene with strong homology to S-100, a calcium-binding protein. J Biol Chem 1986 261 : 12 628 32.
16. Courtois-Coutry N, Le Moellic C, Boulkroun S et al. Calcyclin is an early vasopressin-induced gene in the renal collecting duct. Role in the long term regulation of ion transport. J Biol Chem 2002 277 : 25 728 34.
17. Okazaki K, Niki I, Iino S, Kobayashi S, Hidaka H. A role of calcyclin, a Ca(2+)-binding protein, on the Ca(2+)-dependent insulin release from the pancreatic beta cell. J Biol Chem 1994 269 : 6149 52.
18. Breen EC, Tang K. Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro. J Cell Biochem 2003 88 : 848 54.
19. Filipek A, Jastrzebska B, Nowotny M, Kuznicki J. Cacy BP/SIP, a calcyclin and Siah-1-interacting protein, binds EF-hand proteins of the S100 family. J Biol Chem 2002 277 : 28 848 52.
20. Nowotny M, Spiechowicz M, Jastrzebska B, Filipek A, Kitagawa K, Kuznicki J. Calcium-regulated interaction of Sgt1 with S100A6 (calcyclin) and other S100 proteins. J Biol Chem 2003 278 : 26 923 8.
21. Kuznicki J, Kordowska J, Puzianowska M, Wozniewicz BM. Calcyclin as a marker of human epithelial cells and fibroblasts. Exp Cell Res 1992 200 : 425 30.
22. Filipek A, Puzianowska M, Cieslak B, Kuznicki J. Calcyclin - Ca(2+)-binding protein homologous to glial S-100 beta is present in neurones. Neuroreport 1993 4 : 383 6.
23. Yamashita N, Ilg EC, Schafer BW, Heizmann CW, Kosaka T. Distribution of a specific calcium-binding protein of the S100 protein family, S100A6 (calcyclin), in subpopulations of neurons and glial cells of the adult rat nervous system. J Comp Neurol 1999 404 : 235 57.
24. Luu HH, Zhou L, Haydon RC et al. Increased expression of S100A6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma. Cancer Lett 2005 229 : 135 48.
25. Vimalachandran D, Greenhalf W, Thompson C et al. High nuclear S100A6 (Calcyclin) is significantly associated with poor survival in pancreatic cancer patients. Cancer Res 2005 65 : 3218 25.
26. Shekouh AR, Thompson CC, Prime W et al. Application of laser capture microdissection combined with two-dimensional electrophoresis for the discovery of differentially regulated proteins in pancreatic ductal adenocarcinoma. Proteomics 2003 3 : 1988 2001.
27. Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O. Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int J Cancer 1997 74 : 464 9.
28. Kim J, Kim J, Yoon S et al. S100A6 protein as a marker for differential diagnosis of cholangiocarcinoma from hepatocellular carcinoma. Hepatol Res 2002 23 : 274.
29. Komatsu K, Andoh A, Ishiguro S et al. Increased expression of S100A6 (Calcyclin), a calcium-binding protein of the S100 family, in human colorectal adenocarcinomas. Clin Cancer Res 2000 6 : 172 7.
30. Rehman I, Cross SS, Catto JW et al. Promoter hyper-methylation of calcium binding proteins S100A6 and S100A2 in human prostate cancer. Prostate 2005 65 : 322 30.
31. Crnogorac-Jurcevic T, Missiaglia E, Blaveri E et al. Molecular alterations in pancreatic carcinoma: Expression profiling shows that dysregulated expression of S100 genes is highly prevalent. J Pathol 2003 201 : 63 74.
32. Schafer BW, Wicki R, Engelkamp D, Mattei MG, Heizmann CW. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: Rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics 1995 25 : 638 43.
33. Feng G, Xu X, Youssef EM, Lotan R. Diminished expression of S100A2, a putative tumor suppressor, at early stage of human lung carcinogenesis. Cancer Res 2001 61 : 7999 8004.
34. Wang H, Zhang Z, Li R et al. Overexpression of S100A2 protein as a prognostic marker for patients with stage I non small cell lung cancer. Int J Cancer 2005 116 : 285 90.
35. Zimmer DB, Wright Sadosky P, Weber DJ. Molecular mechanisms of S100-target protein interactions. Microsc Res Techn 2003 60 : 552 9.
36. Spiechowicz M, Zylicz A, Bieganowski P, Kuznicki J, Filipek A. Hsp70 is a new target of Sgt1: An interaction modulated by S100A6. Biochem Biophysl Res Commun 2007 357 : 1148 53.
37. Slomnicki LP, Nawrot B, Lesniak W. S100A6 binds p53 and affects its activity. Int J Biochem Cell Bio 2009 41 : 784 90.
38. Tonini GP, Casalaro A, Cara A, Di Martino D. Inducible expression of calcyclin, a gene with strong homology to S-100 protein, during neuroblastoma cell differentiation and its prevalent expression in Schwann-like cell lines. Cancer Res 1991 51 : 1733 7.
39. Jian Z, Tomizawa Y, Yanagitani N, Iijima H, Sano T, Nakajima T. Papillary adenocarcinoma of the lung is a more advanced adenocarcinoma than bronchioloalveolar carcinoma that is composed of two distinct histological subtypes. Pathol Int 2005 55 : 619 25.
40. Shiseki M, Kohno T, Adachi J et al. Comparative allelotype of early and advanced stage non-small cell lung carcinomas. Genes Chromosomes Cancer 1996 17 : 71 7.
41. Sano T, Kitayama Y, Igarashi H et al. Chromosomal numerical abnormalities in early stage lung adenocarcinoma. Pathol Int 2006 56 : 117 25.
42. Inamura K, Shimoji T, Ninomiya H et al. A metastatic signature in entire lung adenocarcinomas irrespective of morphological heterogeneity. Hum Pathol 2007 38 : 702 9.
43. Ohuchida K, Mizumoto K, Ishikawa N et al. The role of S100A6 in pancreatic cancer development and its clinical implication as a diagnostic marker and therapeutic target. Clin Cancer Res 2005 11 : 7785 93.
44. De Petris L, Orre LM, Kanter L et al. Tumor expression of S100A6 correlates with survival of patients with stage I non-small-cell lung cancer. Lung Cancer 2009 63 : 410 17.
45. Mizuno T, Ishii G, Nagai K et al. Identification of a low risk subgroup of stage IB lung adenocarcinoma patients. Lung Cancer 2008 62 : 302 8.