Proteomic analyses of serous and endometrioid epithelial ovarian cancers - Cases studies - Molecular insights of a possible histological etiology of serous ovarian cancer

Proteomics - Clinical Applications

Volumn 7, Issue 5-6, 2013, Pages 337-354

  Longuespée, Rémi ^a,b   Gagnon, Hugo ^a,b   Boyon, Charlotte ^a,c   Strupat, Kurstin ^d   Dauly, Claire ^e   Kerdraon, Olivier ^c   Ighodaro, Adesuwa ^a,f   Desmons, Annie ^a   Dupuis, Jocelyn ^e   Wisztorski, Maxence ^a   Vinatier, Denis ^a,c   Fournier, Isabelle ^a   Day, Robert ^b   Salzet, Michel ^a  

^a UNIV LILLE   (France)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

^c LILLE UNIVERSITY HOSPITAL   (France)

^d THERMO FISHER SCIENTIFIC   (Germany)

^e Thermo Fisher Scientific   (United States)

^f STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Cases study; MALDI MS imaging; MS profiling; Ovarian cancer; Proteomic network

Indexed keywords

ARTICLE; BENIGN TUMOR; BIOINFORMATICS; CANCER LOCALIZATION; CONTROLLED STUDY; ENDOMETRIOID OVARY CANCER; FALLOPIAN TUBE SEROUS ADENOCARCINOMA; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; OVARY CANCER; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOMICS; SEROUS OVARY CANCER; TANDEM MASS SPECTROMETRY; TISSUE DISTRIBUTION; TUMOR BIOPSY; UTERINE TUBE CARCINOMA;

CARCINOMA, ENDOMETRIOID; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTATIONAL BIOLOGY; CYSTADENOCARCINOMA, SEROUS; FEMALE; HUMANS; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PEPTIDES; PRINCIPAL COMPONENT ANALYSIS; PROTEIN INTERACTION MAPPING; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84879443785     PISSN: 18628346     EISSN: 18628354     Source Type: Journal    
DOI: 10.1002/prca.201200079     Document Type: Article

References (74)

1. Dubeau, L., The cell of origin of ovarian epithelial tumours. Lancet Oncol. 2008, 9, 1191-1197.
2. Shih Ie, M., Kurman, R. J., Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol. 2004, 164, 1511-1518.
3. Bell, D. A., Scully, R. E., Early de novo ovarian carcinoma. A study of fourteen cases. Cancer 1994, 73, 1859-1864.
4. Leblanc, E., Narducci, F., Farre, I., Peyrat, J. P. et al., Radical fimbriectomy: a reasonable temporary risk-reducing surgery for selected women with a germ line mutation of BRCA 1 or 2 genes? Rationale and preliminary development. Gynecol. Oncol. 2011, 121, 472-476.
5. Callahan, M. J., Crum, C. P., Medeiros, F., Kindelberger, D. W. et al., Primary fallopian tube malignancies in BRCA-positive women undergoing surgery for ovarian cancer risk reduction. J. Clin. Oncol. 2007, 25, 3985-3990.
6. Carcangiu, M. L., Radice, P., Manoukian, S., Spatti, G. et al., Atypical epithelial proliferation in fallopian tubes in prophylactic salpingo-oophorectomy specimens from BRCA1 and BRCA2 germline mutation carriers. Int. J. Gynecol. Pathol. 2004, 23, 35-40.
7. Colgan, T. J., Murphy, J., Cole, D. E., Narod, S., Rosen, B., Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status. Am. J. Surg. Pathol. 2001, 25, 1283-1289.
8. Finch, A., Shaw, P., Rosen, B., Murphy, J. et al., Clinical and pathologic findings of prophylactic salpingo-oophorectomies in 159 BRCA1 and BRCA2 carriers. Gynecol. Oncol. 2006, 100, 58-64.
9. Kindelberger, D. W., Lee, Y., Miron, A., Hirsch, M. S., Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am. J. Surg. Pathol. 2007, 31, 161-169.
10. Piek, J. M., van Diest, P. J., Zweemer, R. P., Kenemans, P, Verheijen, R. H., Tubal ligation and risk of ovarian cancer. Lancet 2001, 358, 844.
11. Piek, J. M., Verheijen, R. H., Kenemans, P., Massuger, L. F. et al., BRCA1/2-related ovarian cancers are of tubal origin: a hypothesis. Gynecol. Oncol. 2003, 90, 491.
12. Shaw, P. A., Rouzbahman, M., Pizer, E. S., Pintilie, M., Begley, H., Candidate serous cancer precursors in fallopian tube epithelium of BRCA1/2 mutation carriers. Mod. Pathol. 2009, 22, 1133-1138.
13. Staebler, A., Preneoplasias of ovarian carcinoma: biological and clinical aspects of different pathways of tumorigenesis. Pathologe 2011, 32 (Suppl 2), 265-270.
14. Leonhardt, K., Einenkel, J., Sohr, S., Engeland, K., Horn, L. C., p53 signature and serous tubal in-situ carcinoma in cases of primary tubal and peritoneal carcinomas and serous borderline tumors of the ovary. Int. J. Gynecol. Pathol. 2011, 30, 417-424.
15. Chen, E. Y., Mehra, K., Mehrad, M., Ning, G., Secretory cell outgrowth, PAX2 and serous carcinogenesis in the fallopian tube. J. Pathol. 2011, 222, 110-116.
16. Carlson, J. W., Jarboe, E. A., Kindelberger, D., Nucci, M. R. et al., Serous tubal intraepithelial carcinoma: diagnostic reproducibility and its implications. Int. J. Gynecol. Pathol. 2010, 29, 310-314.
17. Wei, C. F., Hwang, S. H., Ho, C. M., Shih, B. Y., Chien, T. Y., Malignant mixed mullerian tumors of the ovary. Zhonghua Yi Xue Za Zhi (Taipei) 2000, 63, 344-348.
18. Roh, M. H., Kindelberger, D., Crum, C. P., Serous tubal intraepithelial carcinoma and the dominant ovarian mass: clues to serous tumor origin? Am. J. Surg. Pathol. 2009, 33, 376-383.
19. Jarboe, E., Folkins, A., Nucci, M. R., Kindelberger, D. et al., Serous carcinogenesis in the fallopian tube: a descriptive classification. Int. J. Gynecol. Pathol. 2008, 27, 1-9.
20. Stoeckli, M., Chaurand, P., Hallahan, D. E., Caprioli, R. M., Imaging mass spectrometry: a new technology for the analysis of protein expression in mammalian tissues. Nat. Med. 2001, 7, 493-496.
21. Callesen, A. K., Vach, W., Jorgensen, P. E., Cold, S. et al., Reproducibility of mass spectrometry based protein profiles for diagnosis of breast cancer across clinical studies: a systematic review. J. Proteome Res. 2008, 7, 1395-1402.
22. Franck, J., Arafah, K., Elayed, M., Bonnel, D. et al., MALDI imaging mass spectrometry: state of the art technology in clinical proteomics. Mol. Cell. Proteomics 2009, 8, 2023-2033.
23. Schwartz, S. A., Weil, R. J., Thompson, R. C., Shyr, Y. et al., Proteomic-based prognosis of brain tumor patients using direct-tissue matrix-assisted laser desorption ionization mass spectrometry. Cancer Res. 2005, 65, 7674-7681.
24. Fournier, I., Day, R., Salzet, M., Direct analysis of neuropeptides by in situ MALDI-TOF mass spectrometry in the rat brain. Neuro. Endocrinol. Lett. 2003, 24, 9-14.
25. Fournier, I., Wisztorski, M., Salzet, M., Tissue imaging using MALDI-MS: a new frontier of histopathology proteomics. Expert Rev. Proteomics 2008, 5, 413-424.
26. El Ayed, M., Bonnel, D., Longuespee, R., Castellier, C. et al., MALDI imaging mass spectrometry in ovarian cancer for tracking, identifying, and validating biomarkers. Med. Sci. Monit. 2010, 16, BR233-BR245.
27. Franck, J., Longuespee, R., Wisztorski, M., Van Remoortere, A. et al., MALDI mass spectrometry imaging of proteins exceeding 30, 000 daltons. Med. Sci. Monit. 2010, 16, BR293-BR299.
28. Lemaire, R., Lucot, J. P., Collinet, P., Vinatier, D. et al., New developments in direct analyses by MALDI mass spectrometry for study ovarian cancer. Mol. Cell Proteomics 2005, 4, S305-S308.
29. Lemaire, R., Menguellet, S. A., Stauber, J., Marchaudon, V. et al., Specific MALDI imaging and profiling for biomarker hunting and validation: fragment of the 11S proteasome activator complex, Reg alpha fragment, is a new potential ovary cancer biomarker. J. Proteome Res. 2007, 6, 4127-4134.
30. Longuespee, R., Boyon, C., Castellier, C. et al., The C-terminal fragment of the immunoproteasome PA28S (Reg alpha) as an early diagnosis and tumor-relapse biomarker: evidence from mass spectrometry profiling. Histochem Cell Biol. 2012, 138, 141-154.
31. Stauber, J., Lemaire, R., Wisztorski, M., Ait-Menguellet, S. et al., New developments in MALDI imaging mass spectrometry for pathological proteomic studies; introduction to a novel concept, the specific MALDI imaging. Mol. Cell Proteomics 2006, 5, S247-S249.
32. Bonnel, D., Legouffe, R., Willand, N., Baulard, A. et al., MALDI imaging techniques dedicated to drug-distribution studies. Bioanalysis 2011, 3, 1399-1406.
33. Bonnel, D., Longuespee, R., Franck, J., Roudbaraki, M. et al., Multivariate analyses for biomarkers hunting and validation through on-tissue bottom-up or in-source decay in MALDI-MSI: application to prostate cancer. Anal. Bioanal. Chem. 2011, 401, 149-165.
34. Gustafsson, J. O., Oehler, M. K., McColl, S. R., Hoffmann, P., Citric acid antigen retrieval (CAAR) for tryptic peptide imaging directly on archived formalin-fixed paraffin-embedded tissue. J. Proteome Res. 2010, 9, 4315-4328.
35. Franck, J., Arafah, K., Barnes, A., Wisztorski, M. et al., Improving tissue preparation for matrix-assisted laser desorption ionization mass spectrometry imaging. Part 1: using microspotting. Anal. Chem. 2009, 81, 8193-8202.
36. Lemaire, R., Desmons, A., Tabet, J. C., Day, R. et al., Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections. J. Proteome Res. 2007, 6, 1295-1305.
37. Deininger, S. O., Ebert, M. P., Futterer, A., Gerhard, M., Rocken, C., MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers. J. Proteome Res. 2008, 7, 5230-5236.
38. Dauly, C., Fréret, M., Drouot, L., Ho, J. T. C. et al., High-resolution targeted quantitation: biomarker discovery in a mouse transgenic model of myopathy, application note 555, thermo. Fisher Scientific 2011.
39. Colinge, J., Chiappe, D., Lagache, S., Moniatte, M., Bougueleret, L., Differential proteomics via probabilistic peptide identification scores. Anal. Chem. 2005, 77, 596-606.
40. Nanduri, B., Lawrence, M. L., Vanguri, S., Pechan, T., Burgess, S. C., Proteomic analysis using an unfinished bacterial genome: the effects of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 2005, 5, 4852-4863.
41. Searle, B. C., Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 2010, 10, 1265-1269.
42. Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J. et al., Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21, 3674-3676.
43. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M. et al., The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 2011 39, D561-D568.
44. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., Ideker, T., Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27, 431-432.
45. Djidja, M. C., Carolan, V., Loadman, P. M., Clench, M. R., Method development for protein profiling in biological tissues by matrix-assisted laser desorption/ionisation mass spectrometry imaging. Rapid Commun. Mass Spectrom. 2008, 22, 1615-1618.
46. Trim, P. J., Henson, C. M., Avery, J. L., McEwen, A. et al., Matrix-assisted laser desorption/ionization-ion mobility separation-mass spectrometry imaging of vinblastine in whole body tissue sections. Anal. Chem. 2008, 80, 8628-8634.
47. Prat, J., New insights into ovarian cancer pathology. Ann. Oncol. 2012, 23(Suppl 10), x111-x117.
48. Longuespee, R., Boyon, C., Desmons, A. et al., Ovarian cancer molecular pathology. Cancer Metastasis Rev. 2012, 31, 713-732.
49. Longuespee, R., Boyon, C., Castellier, C., Jacquet, A. et al., The C-terminal fragment of the immunoproteasome PA28S (Reg alpha) as an early diagnosis and tumor-relapse biomarker: evidence from mass spectrometry profiling. Histochem. Cell Biol. 2012, 138, 141-154.
50. Ratner, E. S., Keane, F. K., Lindner, R. A., Tassi, R. A. et al., A KRAS variant is a biomarker of poor outcome, platinum chemotherapy resistance and a potential target for therapy in ovarian cancer. Oncogene, 2012, 31, 4559-4566.
51. Meunier, L., Puiffe, M. L., Le Page, C., Filali-Mouhim, A. et al., Effect of ovarian cancer ascites on cell migration and gene expression in an epithelial ovarian cancer in vitro model. Transl. Oncol. 2010, 3, 230-238.
52. Nonaka, M., Itamochi, H., Kawaguchi, W., Kudoh, A. et al., Activation of the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathway overcomes cisplatin resistance in ovarian carcinoma cells. Int. J. Gynecol. Cancer 2012, 22, 922-929.
53. Roberts, P. J., Der, C. J., Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26, 3291-3310.
54. Wilken, J. A., Badri, T., Cross, S., Raji, R. et al., EGFR/HER-targeted therapeutics in ovarian cancer. Future Med. Chem. 2012, 4, 447-469.
55. Felip, E., Del Campo, J. M., Rubio, D., Vidal, M. T. et al., Overexpression of c-erbB-2 in epithelial ovarian cancer. Prognostic value and relationship with response to chemotherapy. Cancer 1995, 75, 2147-2152.
56. Zhou, C., Qiu, L., Sun, Y., Healey, S. et al., Inhibition of EGFR/PI3K/AKT cell survival pathway promotes TSA's effect on cell death and migration in human ovarian cancer cells. Int. J. Oncol. 2006, 29, 269-278.
57. Kandala, P. K., Wright, S. E., Srivastava S. K. Blocking epidermal growth factor receptor activation by 3, 3'-diindolylmethane suppresses ovarian tumor growth in vitro and in vivo. J. Pharmacol. Exp. Ther. 2012, 341, 24-32.
58. Sheng, Q., Liu, J., The therapeutic potential of targeting the EGFR family in epithelial ovarian cancer. Br. J. Cancer 2011, 104, 1241-1245.
59. Judson, P. L., He, X., Cance, W. G., Van Le, L., Overexpression of focal adhesion kinase, a protein tyrosine kinase, in ovarian carcinoma. Cancer 1999, 86, 1551-1556.
60. Xing, H., Weng, D., Chen, G., Tao, W. et al., Activation of fibronectin/PI-3K/Akt2 leads to chemoresistance to docetaxel by regulating survivin protein expression in ovarian and breast cancer cells. Cancer Lett. 2008, 261, 108-119.
61. Vicente-Manzanares, M., Choi, C. K., Horwitz, A. R., Integrins in cell migration-the actin connection. J. Cell Sci. 2009, 122, 199-206.
62. Li, D. Q., Divijendra Natha Reddy, S., Pakala, S. B., Wu, X. et al., MTA1 coregulator regulates p53 stability and function. J. Biol. Chem. 2009, 284, 34545-34552.
63. Creekmore, A. L., Silkworth, W. T., Cimini, D., Jensen, R. V. et al., Changes in gene expression and cellular architecture in an ovarian cancer progression model. PLoS One 2011, 6, e17676.
64. Seeber, L. M., van Diest, P. J., Epigenetics in ovarian cancer. Methods Mol. Biol. 2012, 863, 253-269.
65. Krockenberger, M., Honig, A., Rieger, L., Coy, J. F. et al., Transketolase-like 1 expression correlates with subtypes of ovarian cancer and the presence of distant metastases. Int. J. Gynecol. Cancer 2007, 17, 101-106.
66. Karantanis, D., Allen-Auerbach, M., Czernin, J., Relationship among glycolytic phenotype, grade, and histological subtype in ovarian carcinoma. Clin. Nucl. Med. 2012, 37, 49-53.
67. Grunewald, T. G., Kammerer, U., Winkler, C., Schindler, D. et al., Overexpression of LASP-1 mediates migration and proliferation of human ovarian cancer cells and influences zyxin localisation. Br. J. Cancer 2007, 96, 296-305.
68. Mythreye, K., Blobe, G. C., The type III TGF-beta receptor regulates epithelial and cancer cell migration through beta-arrestin2-mediated activation of Cdc42. Proc. Natl. Acad. Sci. USA 2009, 106, 8221-8216.
69. Chen, J., Xi, B., Zhao, Y., Yu, Y. et al., High-mobility group protein B1 (HMGB1) is a novel biomarker for human ovarian cancer. Gynecol. Oncol. 2012, 126, 109-117.
70. Siu, M. K., Wong, E. S., Chan, H. Y., Kong, D. S. et al., Differential expression and phosphorylation of Pak1 and Pak2 in ovarian cancer: effects on prognosis and cell invasion. Int. J. Cancer 2010, 127, 21-31.
71. Lin, S. W., Ke, F. C., Hsiao, P. W., Lee, P. P. et al., Critical involvement of ILK in TGFbeta1-stimulated invasion/migration of human ovarian cancer cells is associated with urokinase plasminogen activator system. Exp. Cell Res. 2007, 313, 602-613.
72. Gillan, L., Matei, D., Fishman, D. A., Gerbin, C. S. et al., Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res. 2002, 62, 5358-5364.
73. Zhu, M., Fejzo, M. S., Anderson, L., Dering, J. et al., Periostin promotes ovarian cancer angiogenesis and metastasis. Gynecol. Oncol. 2010, 119, 337-344.
74. Kim, K., Visintin, I., Alvero, A. B., Mor, G., Development and validation of a protein-based signature for the detection of ovarian cancer. Clin. Lab. Med. 2009, 29, 47-55.