Serum S100A6 concentration predicts peritoneal tumor burden in mice with epithelial ovarian cancer and is associated with advanced stage in patients

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Wei, Bih Rong ^a   Hoover, Shelley B ^a   Ross, Mark M ^b   Zhou, Weidong ^b   Meani, Francesco ^c   Edwards, Jeniffer B ^a   Spehalski, Elizabeth I ^a,h   Risinger, John I ^d,i   Alvord, W Gregory ^e   Quiñones, Octavio A ^e   Belluco, Claudio ^f,g   Martella, Luca ^f   Campagnutta, Elio ^f   Ravaggi, Antonella ^c   Dai, Rei Ming ^a,e   Goldsmith, Paul K ^a   Woolard, Kevin D ^a   Pecorelli, Sergio ^c   Liotta, Lance A ^b   Petricoin III, Emanuel F ^b   Simpson, R Mark ^a   more..

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

^c UNIVERSITY OF BRESCIA   (Italy)

^d MEMORIAL HEALTH UNIVERSITY MEDICAL CENTER   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^g ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^h UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

ⁱ MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A; BETA ACTIN; BLOOD CLOTTING FACTOR 10; CALCYCLIN; FIBRONECTIN; FRUCTOSE BISPHOSPHATE ALDOLASE; KERATIN TYPE II; LACTATE DEHYDROGENASE; PROTEASOME; TRIOSEPHOSPHATE ISOMERASE; CELL CYCLE PROTEIN; PROTEIN S 100; S100A6 PROTEIN, HUMAN; S100A6 PROTEIN, MOUSE; TUMOR MARKER;

ADVANCED CANCER; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER STAGING; CARCINOMA; CONTROLLED STUDY; DISSEMINATED CANCER; FEMALE; HUMAN; HUMAN TISSUE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; PERITONEUM TUMOR; PREDICTION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEOMICS; TUMOR VOLUME; ADULT; AGED; ANIMAL; BLOOD; CANCER TRANSPLANTATION; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METASTASIS; METHODOLOGY; MIDDLE AGED; NUDE MOUSE; OVARY TUMOR; TUMOR CELL LINE;

ANIMALIA; MUS;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MASS SPECTROMETRY; MICE; MICE, NUDE; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; OVARIAN NEOPLASMS; PROTEOMICS; S100 PROTEINS; TUMOR MARKERS, BIOLOGICAL;

EID: 70449555179     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007670     Document Type: Article

References (56)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
2. Young RC (2003) Early-stage ovarian cancer: to treat or not to treat. J Natl Cancer Inst 95: 94-95.
3. Shih Ie M, Kurman RJ (2004) Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 164: 1511-1518.
4. Cannistra SA (2004) Cancer of the ovary. N Engl J Med 351: 2519-2529.
5. Bast RC, Jr., Siegal FP, Runowicz C, Klug TL, Zurawski VR, Jr., et al. (1985) Elevation of serum CA 125 prior to diagnosis of an epithelial ovarian carcinoma. Gynecol Oncol 22: 115-120.
6. Bast RC, Jr., Knapp RC (1985) Use of the CA 125 antigen in diagnosis and monitoring of ovarian carcinoma. Eur J Obstet Gynecol Reprod Biol 19: 354-356.
7. Williams TI, Toups KL, Saggese DA, Kalli KR, Cliby WA, et al. (2007) Epithelial ovarian cancer: disease etiology, treatment, detection, and investigational gene, metabolite, and protein biomarkers. J Proteome Res 6: 2936-2962.
8. Nossov V, Amneus M, Su F, Lang J, Janco JM, et al. (2008) The early detection of ovarian cancer: from traditional methods to proteomics. Can we really do better than serum CA-125? Am J Obstet Gynecol 199: 215-223.
9. Ahmed FE (2009) Sample preparation and fractionation for proteome analysis and cancer biomarker discovery by mass spectrometry. J Sep Sci 32: 771-798.
10. Faca V, Wang H, Hanash S (2009) Proteomic global profiling for cancer biomarker discovery. Methods Mol Biol 492: 309-320.
11. Luque-Garcia JL, Neubert TA (2007) Sample preparation for serum/plasma profiling and biomarker identification by mass spectrometry. J Chromatogr A 1153: 259-276.
12. Petricoin EF, Belluco C, Araujo RP, Liotta LA (2006) The blood peptidome: a higher dimension of information content for cancer biomarker discovery. Nat Rev Cancer 6: 961-967.
13. Dennis MS, Zhang M, Meng YG, Kadkhodayan M, Kirchhofer D, et al. (2002) Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J Biol Chem 277: 35035-35043.
14. Kurtzhals P, Havelund S, Jonassen I, Kiehr B, Larsen UD, et al. (1995) Albumin binding of insulins acylated with fatty acids: characterization of the ligand-protein interaction and correlation between binding affinity and timing of the insulin effect in vivo. Biochem J 312 ( Pt3): 725-731.
15. Makrides SC, Nygren PA, Andrews B, Ford PJ, Evans KS, et al. (1996) Extended in vivo half-life of human soluble complement receptor type 1 fused to a serum albumin-binding receptor. J Pharmacol Exp Ther 277: 534-542.
16. Kelly-Spratt KS, Kasarda AE, Igra M, Kemp CJ (2008) A mouse model repository for cancer biomarker discovery. J Proteome Res 7: 3613-3618.
17. Hood BL, Lucas DA, Kim G, Chan KC, Blonder J, et al. (2005) Quantitative analysis of the low molecular weight serum proteome using 18O stable isotope labeling in a lung tumor xenograft mouse model. J Am Soc Mass Spectrom 16: 1221-1230.
18. Juan HF, Chen JH, Hsu WT, Huang SC, Chen ST, et al. (2004) Identification of tumor-associated plasma biomarkers using proteomic techniques: from mouse to human. Proteomics 4: 2766-2775.
19. Besada V, Diaz M, Becker M, Ramos Y, Castellanos-Serra L, et al. (2006) Proteomics of xenografted human breast cancer indicates novel targets related to tamoxifen resistance. Proteomics 6: 1038-1048.
20. Rantalainen M, Cloarec O, Beckonert O, Wilson ID, Jackson D, et al. (2006) Statistically integrated metabonomic-proteomic studies on a human prostate cancer xenograft model in mice. J Proteome Res 5: 2642-2655.
21. Zietarska M, Maugard CM, Filali-Mouhim A, Alam-Fahmy M, Tonin PN, et al. (2007) Molecular description of a 3D in vitro model for the study of epithelial ovarian cancer (EOC). Mol Carcinog 46: 872-885.
22. Cross SS, Hamdy FC, Deloulme JC, Rehman I (2005) Expression of S100 proteins in normal human tissues and common cancers using tissue microarrays: S100A6, S100A8, S100A9 and S100A11 are all overexpressed in common cancers. Histopathology 46: 256-269.
23. Filipek A (2006) S100A6 and CacyBP/SIP - two proteins discovered in ehrlich ascites tumor cells that are potentially involved in the degradation of beta-catenin. Chemotherapy 52: 32-34.
24. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450: 191-231.
25. Schaub MC, Heizmann CW (2008) Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 369: 247-264.
26. Schafer BW, Heizmann CW (1996) The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21: 134-140.
27. Donato R (2001) S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 33: 637-668.
28. Kuznicki J, Kordowska J, Puzianowska M, Wozniewicz BM (1992) Calcyclin as a marker of human epithelial cells and fibroblasts. Exp Cell Res 200: 425-430.
29. Vimalachandran D, Greenhalf W, Thompson C, Luttges J, Prime W, et al. (2005) High nuclear S100A6 (Calcyclin) is significantly associated with poor survival in pancreatic cancer patients. Cancer Res 65: 3218-3225.
30. Brown LM, Helmke SM, Hunsucker SW, Netea-Maier RT, Chiang SA, et al. (2006) Quantitative and qualitative differences in protein expression between papillary thyroid carcinoma and normal thyroid tissue. Mol Carcinog 45: 613-626.
31. Ito Y, Yoshida H, Tomoda C, Uruno T, Miya A, et al. (2005) Expression of S100A2 and S100A6 in thyroid carcinomas. Histopathology 46: 569-575.
32. Crnogorac-Jurcevic T, Missiaglia E, Blaveri E, Gangeswaran R, Jones M, et al. (2003) Molecular alterations in pancreatic carcinoma: expression profiling shows that dysregulated expression of S100 genes is highly prevalent. J Pathol 201: 63-74.
33. Ohuchida K, Mizumoto K, Ishikawa N, Fujii K, Konomi H, et al. (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.
34. Komatsu K, Kobune-Fujiwara Y, Andoh A, Ishiguro S, Hunai H, et al. (2000) Increased expression of S100A6 at the invading fronts of the primary lesion and liver metastasis in patients with colorectal adenocarcinoma. Br J Cancer 83: 769-774.
35. De Petris L, Orre LM, Kanter L, Pernemalm M, Koyi H, et al. (2009) Tumor expression of S100A6 correlates with survival of patients with stage I non-small-cell lung cancer. Lung Cancer 63: 410-417.
36. Ohuchida K, Mizumoto K, Yu J, Yamaguchi H, Konomi H, et al. (2007) S100A6 is increased in a stepwise manner during pancreatic carcinogenesis: clinical value of expression analysis in 98 pancreatic juice samples. Cancer Epidemiol Biomarkers Prev 16: 649-654.
37. Luu HH, Zhou L, Haydon RC, Deyrup AT, Montag AG, et al. (2005) Increased expression of S100A6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma. Cancer Lett 229: 135-148.
38. Bast RC, Jr. (2003) Status of tumor markers in ovarian cancer screening. J Clin Oncol 21: 200s-205s.
39. Rapkiewicz AV, Espina V, Petricoin EF, 3rd, Liotta LA (2004) Biomarkers of ovarian tumours. Eur J Cancer 40: 2604-2612.
40. Shan W, Liu J (2009) Epithelial ovarian cancer: focus on genetics and animal models. Cell Cycle 8: 731-735.
41. Petricoin EF, Ardekani AM, Hitt BA, Levine PJ, Fusaro VA, et al. (2002) Use of proteomic patterns in serum to identify ovarian cancer. Lancet 359: 572-577.
42. Rosen DG, Yang G, Liu G, Mercado-Uribe I, Chang B, et al. (2009) Ovarian cancer: pathology, biology, and disease models. Front Biosci 14: 2089-2102.
43. Grote T, Siwak DR, Fritsche HA, Joy C, Mills GB, et al. (2008) Validation of reverse phase protein array for practical screening of potential biomarkers in serum and plasma: accurate detection of CA19-9 levels in pancreatic cancer. Proteomics 8: 3051-3060.
44. Aguilar-Mahecha A, Cantin C, O'Connor-McCourt M, Nantel A, Basik M (2009) Development of reverse phase protein microarrays for the validation of clusterin, a mid-abundant blood biomarker. Proteome Sci 7: 15-27.
45. Camerini S, Polci ML, Liotta LA, Petricoin EF, Zhou W (2007) A method for the selevtive isolation and enrichment of carrier protein-bound low-molecular weight proteins and peptides in the blood. Proteomics Clin Appl 1: 176-184.
46. Wei BR, Edwards JB, Hoover SB, Tillman HS, Reed LT, et al. (2008) Altered {beta}-catenin accumulation in hepatocellular carcinomas of diethylnitrosamine-exposed rhesus macaques. Toxicol Pathol 36: 972-980.
47. Custer MC, Risinger JI, Hoover S, Simpson RM, Patterson T, et al. (2006) Characterization of an antibody that can detect the Kai1/CD82 murine metastasis suppressor. Prostate 66: 567-577.
48. Alvord WG, Rossio JL (1993) Determining confidence limits for drug potency in immunoassay. J Immunol Methods 157: 155-163.
49. DeLean A, Munson PJ, Rodbard D (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Physiol 235: E97-102.
50. Draper NR, Smith H (1998) Applied Regression Analysis. New York: Wiley.
51. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for Mixed Models: SAS Institute, Inc..
52. Milliken GA, Johnson DE (2009) Analysis of Messy Data. New York: Chapman and Hall.
53. (2002-2003) SAS/STAT software. 9.1.3 ed. Cary, NC: SAS Institute Inc.
54. (2005) S-PLUS® 7.0 for Windows. Seattle: WA Insightful Corporation.
55. Team RDC (2008) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
56. Paweletz CP, Charboneau L, Bichsel VE, Simone NL, Chen T, et al. (2001) Reverse phase protein microarrays which capture disease progression show activation of pro-survival pathways at the cancer invasion front. Oncogene 20: 1981-1989.