Tissue-based proteomics reveals FXYD3, S100A11 and GSTM3 as novel markers for regional lymph node metastasis in colon cancer

Journal of Pathology

Volumn 228, Issue 4, 2012, Pages 459-470

  Meding, Stephan ^a   Balluff, Benjamin ^a   Elsner, Mareike ^a   Schöne, Cédrik ^a   Rauser, Sandra ^a   Nitsche, Ulrich ^b   Maak, Matthias ^b   Schäfer, Alexander ^a   Hauck, Stefanie M ^a   Ueffing, Marius ^a,c   Langer, Rupert ^d   Höfler, Heinz ^a,d   Friess, Helmut ^b   Rosenberg, Robert ^b,e   Walch, Axel ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e Kantonsspital Baden   (Switzerland)

Author keywords

Colorectal cancer; Immunohistochemistry; Label free quantitative proteomics; MALDI imaging; Regional lymph node metastasis; Tissue proteomics

Indexed keywords

BIOLOGICAL MARKER; GLUTATHIONE TRANSFERASE M3; PROTEIN FXYD3; PROTEIN S 100; PROTEIN S100A11; UNCLASSIFIED DRUG; FXYD3 PROTEIN, HUMAN; GLUTATHIONE TRANSFERASE; GSTM3 PROTEIN, HUMAN; MEMBRANE PROTEIN; S100A11 PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN; BIOCHEMICAL MARKER; PROTEIN DERIVATIVE;

ADULT; AGED; AMINO ACID SEQUENCE; ARTICLE; COHORT ANALYSIS; COLON CANCER; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; RELIABILITY; TISSUE MICROARRAY; VALIDATION STUDY; COLORECTAL TUMOR; LYMPH NODE; MASS SPECTROMETRY; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; SECONDARY; VERY ELDERLY; CONTROLLED STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ADULT; AGED; AGED, 80 AND OVER; COLORECTAL NEOPLASMS; FEMALE; GLUTATHIONE TRANSFERASE; HUMANS; LYMPH NODES; LYMPHATIC METASTASIS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM PROTEINS; PROGNOSIS; PROTEOMICS; S100 PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUMOR MARKERS, BIOLOGICAL;

EID: 84871194355     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4021     Document Type: Article

References (72)

1. Gunderson LL, Jessup JM, Sargent DJ, et al. Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol 2010; 28: 264-271.
2. Weitz J, Koch M, Debus J, et al. Colorectal cancer. Lancet 2005; 365: 153-165.
3. Meyerhardt JA, Mayer RJ. Systemic therapy for colorectal cancer. N Engl J Med 2005; 352: 476-487.
4. Talmadge JE, Fidler IJ. AACR centennial series: The biology of cancer metastasis: Historical perspective. Cancer Res 2010; 70: 5649-5669.
5. Grade M, Hormann P, Becker S, et al. Gene expression profiling reveals a massive, aneuploidy-dependent transcriptional deregulation and distinct differences between lymph node-negative and lymph node-positive colon carcinomas. Cancer Res 2007; 67: 41-56.
6. Hao JM, Chen JZ, Sui HM, et al. A five-gene signature as a potential predictor of metastasis and survival in colorectal cancer. J Pathol 2010; 220: 475-489.
7. Balluff B, Elsner M, Kowarsch A, et al. Classification of HER2/neu status in gastric cancer using a breast-cancer derived proteome classifier. J Proteome Res 2010; 9: 6317-6322.
8. Seeley EH, Caprioli RM. Molecular imaging of proteins in tissues by mass spectrometry. Proc Natl Acad Sci U S A 2008; 105: 18126-18131.
9. Balluff B, Schone C, Hofler H, et al. MALDI imaging mass spectrometry for direct tissue analysis: Technological advancements and recent applications. Histochem Cell Biol 2011; 136: 227-244.
10. Rauser S, Marquardt C, Balluff B, et al. Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry. J Proteome Res 2010; 9: 1854-1863.
11. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990; 9: 811-818.
12. Gloeckner CJ, Boldt K, Ueffing M. Strep/FLAG tandem affinity purification (SF-TAP) to study protein interactions. Curr Protoc Protein Sci 2009; Chapter 19: Unit19.20.
13. Hauck SM, Dietter J, Kramer RL, et al. Deciphering membraneassociated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol Cell Proteomics 2010; 9: 2292-2305.
14. Oppenheimer SR, Mi D, Sanders M, et al. Molecular analysis of tumor margins by MALDI mass spectrometry in renal carcinoma. J Proteome Res 2010; 9: 2182-2190.
15. Hashimoto Y, Ito T, Inoue H, et al. Prognostic significance of fascin overexpression in human esophageal squamous cell carcinoma. Clin Cancer Res 2005; 11: 2597-2605.
16. Hatakeyama H, Kondo T, Fujii K, et al. Protein clusters associated with carcinogenesis, histological differentiation and nodal metastasis in esophageal cancer. Proteomics 2006; 6: 6300-6316.
17. Tian T, Hao J, Xu A, et al. Determination of metastasis-associated proteins in non-small cell lung cancer by comparative proteomic analysis. Cancer Sci 2007; 98: 1265-1274.
18. Geering K. FXYD proteins: New regulators of Na-K-ATPase. Am J Physiol Renal Physiol 2006; 290: F241-F250.
19. Dairkee SH, Sayeed A, Luciani G, et al. Immutable functional attributes of histologic grade revealed by context-independent gene expression in primary breast cancer cells. Cancer Res 2009; 69: 7826-7834.
20. Kayed H, Kleeff J, Kolb A, et al. FXYD3 is overexpressed in pancreatic ductal adenocarcinoma and influences pancreatic cancer cell growth. Int J Cancer 2006; 118: 43-54.
21. Maxwell PJ, Longley DB, Latif T, et al. Identification of 5- fluorouracil-inducible target genes using cDNA microarray profiling. Cancer Res 2003; 63: 4602-4606.
22. Okudela K, Yazawa T, Ishii J, et al. Down-regulation of FXYD3 expression in human lung cancers: Its mechanism and potential role in carcinogenesis. Am J Pathol 2009; 175: 2646-2656.
23. Widegren E, Onnesjo S, Arbman G, et al. Expression of FXYD3 protein in relation to biological and clinicopathological variables in colorectal cancers. Chemotherapy 2009; 55: 407-413.
24. Yamamoto H, Okumura K, Toshima S, et al. FXYD3 protein involved in tumor cell proliferation is overproduced in human breast cancer tissues. Biol Pharm Bull 2009; 32: 1148-1154.
25. Zhang Z, Pang ST, Kasper KA, et al. FXYD3: A promising biomarker for urothelial carcinoma. Biomark Insights 2011; 6: 17-26.
26. Zhu ZL, Zhao ZR, Zhang Y, et al. Expression and significance of FXYD-3 protein in gastric adenocarcinoma. Dis Markers 2010; 28: 63-69.
27. Loftas P, Onnesjo S, Widegren E, et al. Expression of FXYD-3 is an independent prognostic factor in rectal cancer patients with preoperative radiotherapy. Int J Radiat Oncol Biol Phys 2009; 75: 137-142.
28. He H, Li J, Weng S, et al. S100A11: Diverse function and pathology corresponding to different target proteins. Cell Biochem Biophys 2009; 55: 117-126.
29. Oue N, Hamai Y, Mitani Y, et al. Gene expression profile of gastric carcinoma: Identification of genes and tags potentially involved in invasion, metastasis, and carcinogenesis by serial analysis of gene expression. Cancer Res 2004; 64: 2397-2405.
30. Ohuchida K, Mizumoto K, Ohhashi S, et al. S100A11, a putative tumor suppressor gene, is overexpressed in pancreatic carcinogenesis. Clin Cancer Res 2006; 12: 5417-5422.
31. Lam F, Jankova L, Dent OF, et al. Identification of distinctive protein expression patterns in colorectal adenoma. Proteomics Clin Appl 2010; 4: 60-70.
32. Jung Y, Lee S, Choi HS, et al. Clinical validation of colorectal cancer biomarkers identified from bioinformatics analysis of public expression data. Clin Cancer Res 2011; 17: 700-709.
33. Melle C, Ernst G, Schimmel B, et al. Different expression of calgizzarin (S100A11) in normal colonic epithelium, adenoma and colorectal carcinoma. Int J Oncol 2006; 28: 195-200.
34. Wang G, Wang X, Wang S, et al. Colorectal cancer progression correlates with upregulation of S100A11 expression in tumor tissues. Int J Colorectal Dis 2008; 23: 675-682.
35. Memon AA, Sorensen BS, Meldgaard P, et al. Down-regulation of S100C is associated with bladder cancer progression and poor survival. Clin Cancer Res 2005; 11: 606-611.
36. McKiernan E, McDermott EW, Evoy D, et al. The role of S100 genes in breast cancer progression. Tumour Biol 2011; 32: 441-450.
37. Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol 2005; 45: 51-88.
38. Jain M, Kumar S, Lal P, et al. Role of GSTM3 polymorphism in the risk of developing esophageal cancer. Cancer Epidemiol Biomarkers Prev 2007; 16: 178-181.
39. White DL, Li D, Nurgalieva Z, et al. Genetic variants of glutathione S-transferase as possible risk factors for hepatocellular carcinoma: A HuGE systematic review and meta-analysis. Am J Epidemiol 2008; 167: 377-389.
40. Ye Z, Song H, Higgins JP, et al. Five glutathione S-transferase gene variants in 23,452 cases of lung cancer and 30,397 controls: Meta-analysis of 130 studies. PLoS Med 2006; 3: E91.
41. Holley SL, Rajagopal R, Hoban PR, et al. Polymorphisms in the glutathione S-transferase mu cluster are associated with tumour progression and patient outcome in colorectal cancer. Int J Oncol 2006; 28: 231-236.
42. Loktionov A, Watson MA, Gunter M, et al. Glutathione-Stransferase gene polymorphisms in colorectal cancer patients: Interaction between GSTM1 and GSTM3 allele variants as a riskmodulating factor. Carcinogenesis 2001; 22: 1053-1060.
43. Peng DF, Razvi M, Chen H, et al. DNA hypermethylation regulates the expression of members of the Mu-class glutathione S-transferases and glutathione peroxidases in Barrett's adenocarcinoma. Gut 2009; 58: 5-15.
44. Lim R, Lappas M, Ahmed N, et al. 2D-PAGE of ovarian cancer: Analysis of soluble and insoluble fractions using medium-range immobilized pH gradients. Biochem Biophys Res Commun 2011; 406: 408-413.
45. Mitra AP, Pagliarulo V, Yang D, et al. Generation of a concise gene panel for outcome prediction in urinary bladder cancer. J Clin Oncol 2009; 27: 3929-3937.
46. Song HY, Liu YK, Feng JT, et al. Proteomic analysis on metastasis-associated proteins of human hepatocellular carcinoma tissues. J Cancer Res Clin Oncol 2006; 132: 92-98.
47. Hirasawa Y, Arai M, Imazeki F, et al. Methylation status of genes upregulated by demethylating agent 5-aza-2-deoxycytidine in hepatocellular carcinoma. Oncology 2006; 71: 77-85.
48. Zhou CZ, Qiu GQ, Wang XL, et al. Screening of tumor suppressor genes on 1q31.1-32.1 in Chinese patients with sporadic colorectal cancer. Chin Med J (Engl) 2008; 121: 2479-2486.
49. Martens JW, Nimmrich I, Koenig T, et al. Association of DNA methylation of phosphoserine aminotransferase with response to endocrine therapy in patients with recurrent breast cancer. Cancer Res 2005; 65: 4101-4117.
50. Vie N, Copois V, Bascoul-Mollevi C, et al. Overexpression of phosphoserine aminotransferase PSAT1 stimulates cell growth and increases chemoresistance of colon cancer cells. Mol Cancer 2008; 7: 14.
51. Huang D, Casale GP, Tian J, et al. UDP-glucose dehydrogenase as a novel field-specific candidate biomarker of prostate cancer. Int J Cancer 2010; 126: 315-327.
52. McLaughlin PJ, Stack BC Jr, Levin RJ, et al. Defects in the opioid growth factor receptor in human squamous cell carcinoma of the head and neck. Cancer 2003; 97: 1701-1710.
53. Choi JH, Kim TN, Kim S, et al. Overexpression of mitochondrial thioredoxin reductase and peroxiredoxin III in hepatocellular carcinomas. Anticancer Res 2002; 22: 3331-3335.
54. Kim K, Yu M, Han S, et al. Expression of human peroxiredoxin isoforms in response to cervical carcinogenesis. Oncol Rep 2009; 21: 1391-1396.
55. Basu A, Banerjee H, Rojas H, et al. Differential expression of peroxiredoxins in prostate cancer: Consistent upregulation of PRDX3 and PRDX4. Prostate 2010; 71: 755-765.
56. Holmes JL, Sharp SY, Hobbs S, et al. Silencing of HSP90 cochaperone AHA1 expression decreases client protein activation and increases cellular sensitivity to the HSP90 inhibitor 17-allylamino- 17-demethoxygeldanamycin. Cancer Res 2008; 68: 1188-1197.
57. Garg M, Kanojia D, Saini S, et al. Germ cell-specific heat shock protein 70-2 is expressed in cervical carcinoma and is involved in the growth, migration, and invasion of cervical cells. Cancer 2010; 116: 3785-3796.
58. Milicevic ZT, Petkovic MZ, Drndarevic NC, et al. Expression of heat shock protein 70 (HSP70) in patients with colorectal adenocarcinoma - immunohistochemistry and western blot analysis. Neoplasma 2007; 54: 37-45.
59. Pfister K, Radons J, Busch R, et al. Patient survival by Hsp70 membrane phenotype: Association with different routes of metastasis. Cancer 2007; 110: 926-935.
60. Tsumuraya M, Kato H, Miyachi K, et al. Comprehensive analysis of genes involved in the malignancy of gastrointestinal stromal tumors. Anticancer Res 2010; 30: 2705-2715.
61. Stewart GD, Skipworth RJ, Pennington CJ, et al. Variation in dermcidin expression in a range of primary human tumours and in hypoxic/oxidatively stressed human cell lines. Br J Cancer 2008; 99: 126-132.
62. Park HJ, Kim BG, Lee SJ, et al. Proteomic profiling of endothelial cells in human lung cancer. J Proteome Res 2008; 7: 1138-1150.
63. Schulz DM, Bollner C, Thomas G, et al. Identification of differentially expressed proteins in triple-negative breast carcinomas using DIGE and mass spectrometry. J Proteome Res 2009; 8: 3430-3438.
64. Trojanowicz B, Sekulla C, Lorenz K, et al. Proteomic approach reveals novel targets for retinoic acid-mediated therapy of thyroid carcinoma. Mol Cell Endocrinol 2010; 325: 110-117.
65. Wiese AH, Auer J, Lassmann S, et al. Identification of gene signatures for invasive colorectal tumor cells. Cancer Detect Prev 2007; 31: 282-295.
66. Qi W, Liu X, Qiao D, et al. Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int J Cancer 2005; 113: 359-363.
67. Pereira-Faca SR, Kuick R, Puravs E, et al. Identification of 14-3-3 theta as an antigen that induces a humoral response in lung cancer. Cancer Res 2007; 67: 12000-12006.
68. Bai Z, Ye Y, Liang B, et al. Proteomics-based identification of a group of apoptosis-related proteins and biomarkers in gastric cancer. Int J Oncol 2011; 38: 375-383.
69. Yoder BJ, Tso E, Skacel M, et al. The expression of fascin, an actin-bundling motility protein, correlates with hormone receptornegative breast cancer and a more aggressive clinical course. Clin Cancer Res 2005; 11: 186-192.
70. Darnel AD, Behmoaram E, Vollmer RT, et al. Fascin regulates prostate cancer cell invasion and is associated with metastasis and biochemical failure in prostate cancer. Clin Cancer Res 2009; 15: 1376-1383.
71. Ozerhan IH, Ersoz N, Onguru O, et al. Fascin expression in colorectal carcinomas. Clinics (Sao Paulo) 2010; 65: 157-164.
72. Sudarshan S, Shanmugasundaram K, Naylor SL, et al. Reduced expression of fumarate hydratase in clear cell renal cancer mediates HIF-2alpha accumulation and promotes migration and invasion. PLoS One 2011; 6: E21037.