Proteomic and PROTEOMEX profiling of mammary cancer progression in a HER-2/neu oncogene-driven animal model system

Proteomics

Volumn 10, Issue 21, 2010, Pages 3835-3853

  Croci, Stefania ^a   Recktenwald, Christian V ^b   Lichtenfels, Rudolf ^b   Nicoletti, Giordano ^c   Dressler, Sven P ^b   De Giovanni, Carla ^a   Astolfi, Annalisa ^a   Palladini, Arianna ^a   Shin Ya, Kazuo ^d   Landuzzi, Lorena ^c   Nanni, Patrizia ^a   Lollini, Pier Luigi ^a   Seliger, Barbara ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Autoantibody; Cell biology; Immunoprevention; Mammary cancer; Transgenic mice; Vaccine

Indexed keywords

AUTOANTIBODY; CALPHOBINDIN II; CHAPERONE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLUCOSE REGULATED PROTEIN 78; IMMUNOGLOBULIN G ANTIBODY; MITOMYCIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER PREVENTION; CARCINOGENESIS; CELL GROWTH; CELL MOTILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; IMMUNOPRECIPITATION; MAMMARY GLAND; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; TRANSCRIPTOMICS; TUMOR GROWTH; UPREGULATION; VACCINATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, NEOPLASM; AUTOANTIBODIES; CANCER VACCINES; CELL LINE, TUMOR; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION PROFILING; HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; IMMUNOGLOBULIN G; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; RECEPTOR, ERBB-2; REPRODUCIBILITY OF RESULTS;

ANIMALIA; MURINAE; MUS; MUS MUSCULUS;

EID: 78049381358     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200900643     Document Type: Article

References (70)

1. Lollini, P. L., Cavallo, F., Nanni, P., Forni, G., Vaccines for tumour prevention. Nat. Rev. Cancer 2006, 6, 204-216.
2. De Giovanni, C., Nicoletti, G., Landuzzi, L., Astolfi, A. et al., Immunoprevention of HER-2/neu transgenic mammary carcinoma through an interleukin 12-engineered allogeneic cell vaccine. Cancer Res. 2004, 64, 4001-4009.
3. Nanni, P., Nicoletti, G., De Giovanni, C., Landuzzi, L. et al., Combined allogeneic tumor cell vaccination and systemic interleukin 12 prevents mammary carcinogenesis in HER-2/neu transgenic mice. J. Exp. Med. 2001, 194, 1195-1205.
4. Ursini-Siegel, J., Schade, B., Cardiff, R. D., Muller, W. J., Insights from transgenic mouse models of ERBB2-induced breast cancer. Nat. Rev. Cancer 2007, 7, 389-397.
5. Moasser, M. M., The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene 2007, 26, 6469-6487.
6. Nanni, P., Landuzzi, L., Nicoletti, G., De Giovanni, C. et al., Immunoprevention of mammary carcinoma in HER-2/neu transgenic mice is IFN-gamma and B cell dependent. J. Immunol. 2004, 173, 2288-2296.
7. Pilon, S. A., Kelly, C., Wei, W. Z., Broadening of epitope recognition during immune rejection of ErbB-2-positive tumor prevents growth of ErbB-2-negative tumor. J. Immunol. 2003, 170, 1202-1208.
8. Rauch, J., Gires, O., SEREX, Proteomex, AMIDA, and beyond: serological screening technologies for target identification. Proteomics Clin. Appl. 2008, 2, 355-371.
9. Jungblut, P. R., Grabher, G., Stoffler, G., Comprehensive detection of immunorelevant Borrelia garinii antigens by two-dimensional electrophoresis. Electrophoresis 1999, 20, 3611-3622.
10. Brichory, F., Beer, D., Le Naour, F., Giordano, T., Hanash, S., Proteomics-based identification of protein gene product 9.5 as a tumor antigen that induces a humoral immune response in lung cancer. Cancer Res. 2001, 61, 7908-7912.
11. Desmetz, C., Bibeau, F., Boissiere, F., Bellet, V. et al., Proteomics-based identification of HSP60 as a tumor-associated antigen in early stage breast cancer and ductal carcinoma in situ. J. Proteome Res. 2008, 7, 3830-3837.
12. Fujita, Y., Nakanishi, T., Hiramatsu, M., Mabuchi, H. et al., Proteomics-based approach identifying autoantibody against peroxiredoxin VI as a novel serum marker in esophageal squamous cell carcinoma. Clin. Cancer Res. 2006, 12, 6415-6420.
13. Hamrita, B., Chahed, K., Kabbage, M., Guillier, C. L. et al., Identification of tumor antigens that elicit a humoral immune response in breast cancer patients' sera by serological proteome analysis (SERPA). Clin. Chim. Acta 2008, 393, 95-102.
14. Hanash, S., Brichory, F., Beer, D., A proteomic approach to the identification of lung cancer markers. Dis. Markers 2001, 17, 295-300.
15. Hong, S. H., Misek, D. E., Wang, H., Puravs, E. et al., Identification of a specific vimentin isoform that induces an antibody response in pancreatic cancer. Biomark. Insights 2006, 1, 175-183.
16. Klade, C. S., Voss, T., Krystek, E., Ahorn, H. et al., Identification of tumor antigens in renal cell carcinoma by serological proteome analysis. Proteomics 2001, 1, 890-898.
17. Le Naour, F., Brichory, F., Misek, D. E., Brechot, C. et al., A distinct repertoire of autoantibodies in hepatocellular carcinoma identified by proteomic analysis. Mol. Cell. Proteomics 2002, 1, 197-203.
18. Le Naour, F., Misek, D. E., Krause, M. C., Deneux, L. et al., Proteomics-based identification of RS/DJ-1 as a novel circulating tumor antigen in breast cancer. Clin. Cancer Res. 2001, 7, 3328-3335.
19. Li, C., Xiao, Z., Chen, Z., Zhang, X. et al., Proteome analysis of human lung squamous carcinoma. Proteomics 2006, 6, 547-558.
20. Lichtenfels, R., Kellner, R., Atkins, D., Bukur, J. et al., Identification of metabolic enzymes in renal cell carcinoma utilizing PROTEOMEX analyses. Biochim. Biophys. Acta 2003, 1646, 21-31.
21. Lichtenfels, R., Kellner, R., Bukur, J., Beck, J. et al., Heat shock protein expression and anti-heat shock protein reactivity in renal cell carcinoma. Proteomics 2002, 2, 561-570.
22. Prasannan, L., Misek, D. E., Hinderer, R., Michon, J. et al., Identification of beta-tubulin isoforms as tumor antigens in neuroblastoma. Clin. Cancer Res. 2000, 6, 3949-3956.
23. Shalhoub, P., Kern, S., Girard, S., Beretta, L., Proteomic-based approach for the identification of tumor markers associated with hepatocellular carcinoma. Dis. Markers 2001, 17, 217-223.
24. Tomaino, B., Cappello, P., Capello, M., Fredolini, C. et al., Autoantibody signature in human ductal pancreatic adenocarcinoma. J. Proteome Res. 2007, 6, 4025-4031.
25. Unwin, R. D., Harnden, P., Pappin, D., Rahman, D. et al., Serological and proteomic evaluation of antibody responses in the identification of tumor antigens in renal cell carcinoma. Proteomics 2003, 3, 45-55.
26. Yang, F., Xiao, Z. Q., Zhang, X. Z., Li, C. et al., Identification of tumor antigens in human lung squamous carcinoma by serological proteome analysis. J. Proteome Res. 2007, 6, 751-758.
27. Astolfi, A., Landuzzi, L., Nicoletti, G., De Giovanni, C. et al., Gene expression analysis of immune-mediated arrest of tumorigenesis in a transgenic mouse model of HER-2/neu-positive basal-like mammary carcinoma. Am. J. Pathol. 2005, 166, 1205-1216.
28. Wulfkuhle, J. D., Sgroi, D. C., Krutzsch, H., McLean, K. et al., Proteomics of human breast ductal carcinoma in situ. Cancer Res. 2002, 62, 6740-6749.
29. Ramagli, L. S., Rodriguez, L. V., Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 1985, 6, 559-563.
30. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996, 68, 850-858.
31. Neuhoff, V., Stamm, R., Eible, H., Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels: a systematic analysis. Electrophoresis 1985, 6, 427-448.
32. Recktenwald, C. V., Kellner, R., Lichtenfels, R., Seliger, B., Altered detoxification status and increased resistance to oxidative stress by K-ras transformation. Cancer Res. 2008, 68, 10086-10093.
33. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S., Mische, S. M., Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 1999, 20, 601-605.
34. Lichtenfels, R., Ackermann, A., Kellner, R., Seliger, B., Mapping and expression pattern analysis of key components of the major histocompatibility complex class I antigen processing and presentation pathway in a representative human renal cell carcinoma cell line. Electrophoresis 2001, 22, 1801-1809.
35. Park, H. R., Tomida, A., Sato, S., Tsukumo, Y. et al., Effect on tumor cells of blocking survival response to glucose deprivation. J. Natl. Cancer Inst. 2004, 96, 1300-1310.
36. Di Carlo, E., Diodoro, M. G., Boggio, K., Modesti, A. et al., Analysis of mammary carcinoma onset and progression in HER-2/neu oncogene transgenic mice reveals a lobular origin. Lab. Invest. 1999, 79, 1261-1269.
37. Quaglino, E., Rolla, S., Iezzi, M., Spadaro, M. et al., Concordant morphologic and gene expression data show that a vaccine halts HER-2/neu preneoplastic lesions. J. Clin. Invest. 2004, 113, 709-717.
38. Calogero, R. A., Cordero, F., Forni, G., Cavallo, F., Inflammation and breast cancer. Inflammatory component of mammary carcinogenesis in ErbB2 transgenic mice. Breast Cancer Res. 2007, 9, 211.
39. Brockmann, R., Beyer, A., Heinisch, J. J., Wilhelm, T., Posttranscriptional expression regulation: what determines translation rates? PLoS Comput. Biol. 2007, 3, e57.
40. Hollinshead, M., Sanderson, J., Vaux, D. J., Anti-biotin antibodies offer superior organelle-specific labeling of mitochondria over avidin or streptavidin. J. Histochem. Cytochem. 1997, 45, 1053-1057.
41. Finn, O. J., Premalignant lesions as targets for cancer vaccines. J. Exp. Med. 2003, 198, 1623-1626.
42. Aksu, S., Scheler, C., Focks, N., Leenders, F. et al., An iterative calibration method with prediction of post-translational modifications for the construction of a two-dimensional electrophoresis database of mouse mammary gland proteins. Proteomics 2002, 2, 1452-1463.
43. Elliott, B. E., Meens, J. A., SenGupta, S. K., Louvard, D., Arpin, M., The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells. Breast Cancer Res. 2005, 7, R365-R373.
44. Honda, K., Yamada, T., Endo, R., Ino, Y. et al., Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion. J. Cell Biol. 1998, 140, 1383-1393.
45. Fernandez, P. M., Tabbara, S. O., Jacobs, L. K., Manning, F. C. et al., Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res. Treat. 2000, 59, 15-26.
46. Gazit, G., Lu, J., Lee, A. S., De-regulation of GRP stress protein expression in human breast cancer cell lines. Breast Cancer Res. Treat. 1999, 54, 135-146.
47. Fu, Y., Lee, A. S., Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol. Ther. 2006, 5, 741-744.
48. Gonzalez-Gronow, M., Cuchacovich, M., Llanos, C., Urzua, C. et al., Prostate cancer cell proliferation in vitro is modulated by antibodies against glucose-regulated protein 78 isolated from patient serum. Cancer Res. 2006, 66, 11424-11431.
49. Dong, D., Ni, M., Li, J., Xiong, S. et al., Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res. 2008, 68, 498-505.
50. Arap, M. A., Lahdenranta, J., Mintz, P. J., Hajitou, A. et al., Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 2004, 6, 275-284.
51. Chavany, C., Mimnaugh, E., Miller, P., Bitton, R. et al., p185erbB2 binds to GRP94 in vivo. Dissociation of the p185erbB2/GRP94 heterocomplex by benzoquinone ansamycins precedes depletion of p185erbB2. J. Biol. Chem. 1996, 271, 4974-4977.
52. Jakobsen, C. G., Rasmussen, N., Laenkholm, A. V., Ditzel, H. J., Phage display derived human monoclonal antibodies isolated by binding to the surface of live primary breast cancer cells recognize GRP78. Cancer Res. 2007, 67, 9507-9517.
53. Triantafilou, M., Fradelizi, D., Triantafilou, K., Major histocompatibility class one molecule associates with glucose regulated protein (GRP) 78 on the cell surface. Hum. Immunol. 2001, 62, 764-770.
54. Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., Schreiber, R. D., Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 2002, 3, 991-998.
55. Street, S. E., Zerafa, N., Iezzi, M., Westwood, J. A. et al., Host perforin reduces tumor number but does not increase survival in oncogene-driven mammary adenocarcinoma. Cancer Res. 2007, 67, 5454-5460.
56. Ambrosino, E., Spadaro, M., Iezzi, M., Curcio, C. et al., Immunosurveillance of Erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell self-tolerance. Cancer Res. 2006, 66, 7734-7740.
57. Melani, C., Chiodoni, C., Forni, G., Colombo, M. P., Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 2003, 102, 2138-2145.
58. Iyengar, P., Espina, V., Williams, T. W., Lin, Y. et al., Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J. Clin. Invest. 2005, 115, 1163-1176.
59. Coronella-Wood, J. A., Hersh, E. M., Naturally occurring B-cell responses to breast cancer. Cancer Immunol. Immunother. 2003, 52, 715-738.
60. Lu, H., Knutson, K. L., Gad, E., Disis, M. L., The tumor antigen repertoire identified in tumor-bearing neu transgenic mice predicts human tumor antigens. Cancer Res. 2006, 66, 9754-9761.
61. Berghs, S., Ferracci, F., Maksimova, E., Gleason, S. et al., Autoimmunity to beta IV spectrin in paraneoplastic lower motor neuron syndrome. Proc. Natl. Acad. Sci. USA 2001, 98, 6945-6950.
62. de Visser, K. E., Eichten, A., Coussens, L. M., Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 2006, 6, 24-37.
63. Tan, T. T., Coussens, L. M., Humoral immunity, inflammation and cancer. Curr. Opin. Immunol. 2007, 19, 209-216.
64. Mizoguchi, A., Bhan, A. K., A case for regulatory B cells. J. Immunol. 2006, 176, 705-710.
65. Inoue, F., Zhang, Q., Akiyoshi, T., Aramaki, O. et al., Prolongation of survival of fully allogeneic cardiac grafts and generation of regulatory cells by a histamine receptor 2 antagonist. Transplantation 2007, 84, 1288-1297.
66. Tesniere, A., Panaretakis, T., Kepp, O., Apetoh, L. et al., Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 2008, 15, 3-12.
67. Preiss, S., Kammertoens, T., Lampert, C., Willimsky, G., Blankenstein, T., Tumor-induced antibodies resemble the response to tissue damage. Int. J. Cancer 2005, 115, 456-462.
68. Gerke, V., Creutz, C. E., Moss, S. E., Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6, 449-461.
69. Bode, G., Luken, A., Kerkhoff, C., Roth, J. et al., Interaction between S100A8/A9 and annexin A6 is involved in the calcium-induced cell surface exposition of S100A8/A9. J. Biol. Chem. 2008, 283, 31776-31784.
70. Vila de Muga, S., Timpson, P., Cubells, L., Evans, R. et al., Annexin A6 inhibits Ras signalling in breast cancer cells. Oncogene 2009, 28, 363-377.