Submit
Search
Submit
Menu

  • Information

  • References

  • Contents

  • [1]D. Pardoll: Cancer and the Immune System: Basic Concepts and Targets for Intervention. Semin Oncol, 42(4), 523-38 (2015)

  • [2]L. Gross: Intradermal immunization of C3H mice against a sarcoma that originated in an animal of the same line. Cancer Res, 3, 326–333 (1943)

  • [3]T. Boon and A. Van Pel: Teratocarcinoma cell variants rejected by syngeneic mice: protection of mice immunized with these variants against other variants and against the original malignant cell line. Proc Natl Acad Sci U S A, 75(3), 1519-23 (1978)

  • [4]A. Van Pel and T. Boon: Protection against a nonimmunogenic mouse leukemia by an immunogenic variant obtained by mutagenesis. Proc Natl Acad Sci U S A, 79(15), 4718-22 (1982)

  • [5]P. G. Coulie, B. J. Van den Eynde, P. van der Bruggen and T. Boon: Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer, 14(2), 135-46 (2014)

  • [6]P. O. Livingston, H. Shiku, M. A. Bean, C. M. Pinsky, H. F. Oettgen and L. J. Old: Cell-mediated cytotoxicity for cultured autologous melanoma cells. Int J Cancer, 24(1), 34-44 (1979)

  • [7]A. Knuth, B. Danowski, H. F. Oettgen and L. J. Old: T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc Natl Acad Sci U S A, 81(11), 3511-5 (1984)

  • [8]S. A. Rosenberg, B. S. Packard, P. M. Aebersold, D. Solomon, S. L. Topalian, S. T. Toy, P. Simon, M. T. Lotze, J. C. Yang, C. A. Seipp and et al.: Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med, 319(25), 1676-80 (1988)

  • [9]M. Herin, C. Lemoine, P. Weynants, F. Vessiere, A. Van Pel, A. Knuth, R. Devos and T. Boon: Production of stable cytolytic T-cell clones directed against autologous human melanoma. Int J Cancer, 39(3), 390-6 (1987)

  • [10]U. Sahin, O. Tureci, H. Schmitt, B. Cochlovius, T. Johannes, R. Schmits, F. Stenner, G. Luo, I. Schobert and M. Pfreundschuh: Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Natl Acad Sci U S A, 92(25), 11810-3 (1995)

  • [11]U. Sahin, O. Tureci and M. Pfreundschuh: Serological identification of human tumor antigens. Curr Opin Immunol, 9(5), 709-16 (1997)

  • [12]L. J. Old and Y. T. Chen: New paths in human cancer serology. J Exp Med, 187(8), 1163-7 (1998)

  • [13]F. Le Naour: Contribution of proteomics to tumor immunology. Proteomics, 1(10), 1295-302 (2001)

  • [14]O. Tureci, U. Sahin and M. Pfreundschuh: Serological analysis of human tumor antigens: molecular definition and implications. Mol Med Today, 3(8), 342-9 (1997)

  • [15]B. Tomaino, P. Cappello, M. Capello, C. Fredolini, A. Ponzetto, A. Novarino, L. Ciuffreda, O. Bertetto, C. De Angelis, E. Gaia, P. Salacone, M. Milella, P. Nistico, M. Alessio, R. Chiarle, M. G. Giuffrida, M. Giovarelli and F. Novelli: Autoantibody signature in human ductal pancreatic adenocarcinoma. J Proteome Res, 6(10), 4025-31 (2007)

  • [16]M. Capello, S. Ferri-Borgogno, P. Cappello and F. Novelli: alpha-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J, 278(7), 1064-74 (2011)

  • [17]B. Altenberg and K. O. Greulich: Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics, 84(6), 1014-20 (2004)

  • [18]Y. Song, Q. Luo, H. Long, Z. Hu, T. Que, X. Zhang, Z. Li, G. Wang, L. Yi, Z. Liu, W. Fang and S. Qi: Alpha-enolase as a potential cancer prognostic marker promotes cell growth, migration, and invasion in glioma. Mol Cancer, 13, 65 (2014)

  • [19]S. H. Tu, C. C. Chang, C. S. Chen, K. W. Tam, Y. J. Wang, C. H. Lee, H. W. Lin, T. C. Cheng, C. S. Huang, J. S. Chu, N. Y. Shih, L. C. Chen, S. J. Leu, Y. S. Ho and C. H. Wu: Increased expression of enolase alpha in human breast cancer confers tamoxifen resistance in human breast cancer cells. Breast Cancer Res Treat, 121(3), 539-53 (2010)

  • [20]R. I. Somiari, A. Sullivan, S. Russell, S. Somiari, H. Hu, R. Jordan, A. George, R. Katenhusen, A. Buchowiecka, C. Arciero, H. Brzeski, J. Hooke and C. Shriver: High-throughput proteomic analysis of human infiltrating ductal carcinoma of the breast. Proteomics, 3(10), 1863-73 (2003)

  • [21]M. Kabbage, K. Chahed, B. Hamrita, C. L. Guillier, M. Trimeche, S. Remadi, J. Hoebeke and L. Chouchane: Protein alterations in infiltrating ductal carcinomas of the breast as detected by nonequilibrium pH gradient electrophoresis and mass spectrometry. J Biomed Biotechnol, 2008, 564127 (2008)

  • [22]L. Malorni, G. Cacace, M. Cuccurullo, G. Pocsfalvi, A. Chambery, A. Farina, A. Di Maro, A. Parente and A. Malorni: Proteomic analysis of MCF-7 breast cancer cell line exposed to mitogenic concentration of 17beta-estradiol. Proteomics, 6(22), 5973-82 (2006)

  • [23]A. Hennipman, B. A. van Oirschot, J. Smits, G. Rijksen and G. E. Staal: Glycolytic enzyme activities in breast cancer metastases. Tumour Biol, 9(5), 241-8 (1988)

  • [24]A. Hennipman, J. Smits, B. van Oirschot, J. C. van Houwelingen, G. Rijksen, J. P. Neyt, J. A. Van Unnik and G. E. Staal: Glycolytic enzymes in breast cancer, benign breast disease and normal breast tissue. Tumour Biol, 8(5), 251-63 (1987)

  • [25]H. Zhou, C. B. Chen, J. Lan, C. Liu, X. G. Liu, L. Jiang, F. Wei, Q. J. Ma, G. T. Dang and Z. J. Liu: Differential proteomic profiling of chordomas and analysis of prognostic factors. J Surg Oncol, 102(7), 720-7 (2010)

  • [26]S. M. Bae, H. J. Min, G. H. Ding, S. Y. Kwak, Y. L. Cho, K. H. Nam, C. H. Park, Y. W. Kim, C. K. Kim, B. D. Han, Y. J. Lee, D. K. Kim and W. S. Ahn: Protein expression profile using two-dimensional gel analysis in squamous cervical cancer patients. Cancer Res Treat, 38(2), 99-107 (2006)

  • [27]S. M. Bae, C. H. Lee, Y. L. Cho, K. H. Nam, Y. W. Kim, C. K. Kim, B. D. Han, Y. J. Lee, H. J. Chun and W. S. Ahn: Two-dimensional gel analysis of protein expression profile in squamous cervical cancer patients. Gynecol Oncol, 99(1), 26-35 (2005)

  • [28]M. Katayama, H. Nakano, A. Ishiuchi, W. Wu, R. Oshima, J. Sakurai, H. Nishikawa, S. Yamaguchi and T. Otsubo: Protein pattern difference in the colon cancer cell lines examined by two-dimensional differential in-gel electrophoresis and mass spectrometry. Surg Today, 36(12), 1085-93 (2006)

  • [29]C. S. Wong, V. W. Wong, C. M. Chan, B. B. Ma, E. P. Hui, M. C. Wong, M. Y. Lam, T. C. Au, W. H. Chan, W. Cheuk and A. T. Chan: Identification of 5-fluorouracil response proteins in colorectal carcinoma cell line SW480 by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Oncol Rep, 20(1), 89-98 (2008)

  • [30]Y. Qi, J. F. Chiu, L. Wang, D. L. Kwong and Q. Y. He: Comparative proteomic analysis of esophageal squamous cell carcinoma. Proteomics, 5(11), 2960-71 (2005)

  • [31]J. Zhao, A. C. Chang, C. Li, K. A. Shedden, D. G. Thomas, D. E. Misek, A. P. Manoharan, T. J. Giordano, D. G. Beer and D. M. Lubman: Comparative proteomics analysis of Barrett metaplasia and esophageal adenocarcinoma using two-dimensional liquid mass mapping. Mol Cell Proteomics, 6(6), 987-99 (2007)

  • [32]R. B. Govekar, A. K. D’Cruz, K. Alok Pathak, J. Agarwal, K. A. Dinshaw, R. F. Chinoy, N. Gadewal, S. Kannan, R. Sirdeshmukh, C. S. Sundaram, S. A. Malgundkar, S. V. Kane and S. M. Zingde: Proteomic profiling of cancer of the gingivo-buccal complex: Identification of new differentially expressed markers. Proteomics Clin Appl, 3(12), 1451-62 (2009)

  • [33]S. T. Tsai, I. H. Chien, W. H. Shen, Y. Z. Kuo, Y. T. Jin, T. Y. Wong, J. R. Hsiao, H. P. Wang, N. Y. Shih and L. W. Wu: ENO1, a potential prognostic head and neck cancer marker, promotes transformation partly via chemokine CCL20 induction. Eur J Cancer, 46(9), 1712-23 (2010)

  • [34]N. M. White-Al Habeeb, A. Di Meo, A. Scorilas, F. Rotondo, O. Masui, A. Seivwright, M. Gabril, A. H. Girgis, M. A. Jewett and G. M. Yousef: Alpha-enolase is a potential prognostic marker in clear cell renal cell carcinoma. Clin Exp Metastasis, 32(6), 531-41 (2015)

  • [35]C. Lopez-Pedrera, J. M. Villalba, E. Siendones, N. Barbarroja, C. Gomez-Diaz, A. Rodriguez-Ariza, P. Buendia, A. Torres and F. Velasco: Proteomic analysis of acute myeloid leukemia: Identification of potential early biomarkers and therapeutic targets. Proteomics, 6 Suppl 1, S293-9 (2006)

  • [36]T. Hamaguchi, N. Iizuka, R. Tsunedomi, Y. Hamamoto, T. Miyamoto, M. Iida, Y. Tokuhisa, K. Sakamoto, M. Takashima, T. Tamesa and M. Oka: Glycolysis module activated by hypoxia-inducible factor 1 alpha is related to the aggressive phenotype of hepatocellular carcinoma. Int J Oncol, 33(4), 725-31 (2008)

  • [37]M. Takashima, Y. Kuramitsu, Y. Yokoyama, N. Iizuka, M. Fujimoto, T. Nishisaka, K. Okita, M. Oka and K. Nakamura: Overexpression of alpha enolase in hepatitis C virus-related hepatocellular carcinoma: association with tumor progression as determined by proteomic analysis. Proteomics, 5(6), 1686-92 (2005)

  • [38]L. S. Li, H. Kim, H. Rhee, S. H. Kim, D. H. Shin, K. Y. Chung, K. S. Park, Y. K. Paik and J. Chang: Proteomic analysis distinguishes basaloid carcinoma as a distinct subtype of nonsmall cell lung carcinoma. Proteomics, 4(11), 3394-400 (2004)

  • [39]C. Li, Z. Xiao, Z. Chen, X. Zhang, J. Li, X. Wu, X. Li, H. Yi, M. Li, G. Zhu and S. Liang: Proteome analysis of human lung squamous carcinoma. Proteomics, 6(2), 547-58 (2006)

  • [40]L. J. Huang, S. X. Chen, W. J. Luo, H. H. Jiang, P. F. Zhang and H. Yi: Proteomic analysis of secreted proteins of non-small cell lung cancer. Ai Zheng, 25(11), 1361-7 (2006)

  • [41]A. Rubporn, C. Srisomsap, P. Subhasitanont, D. Chokchaichamnankit, K. Chiablaem, J. Svasti and P. Sangvanich: Comparative proteomic analysis of lung cancer cell line and lung fibroblast cell line. Cancer Genomics Proteomics, 6(4), 229-37 (2009)

  • [42]G. C. Chang, K. J. Liu, C. L. Hsieh, T. S. Hu, S. Charoenfuprasert, H. K. Liu, K. T. Luh, L. H. Hsu, C. W. Wu, C. C. Ting, C. Y. Chen, K. C. Chen, T. Y. Yang, T. Y. Chou, W. H. Wang, J. Whang-Peng and N. Y. Shih: Identification of alpha-enolase as an autoantigen in lung cancer: its overexpression is associated with clinical outcomes. Clin Cancer Res, 12(19), 5746-54 (2006)

  • [43]K. C. Hsiao, N. Y. Shih, H. L. Fang, T. S. Huang, C. C. Kuo, P. Y. Chu, Y. M. Hung, S. W. Chou, Y. Y. Yang, G. C. Chang and K. J. Liu: Surface alpha-enolase promotes extracellular matrix degradation and tumor metastasis and represents a new therapeutic target. PLoS One, 8(7), e69354 (2013)

  • [44]L. Cao, X. Li, Y. Zhang, F. Peng, H. Yi, Y. Xu and Q. Wang: Proteomic analysis of human ovarian cancer paclitaxel-resistant cell lines. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 35(4), 286-94 (2010)

  • [45]J. Shen, M. D. Person, J. Zhu, J. L. Abbruzzese and D. Li: Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by two-dimensional gel electrophoresis and mass spectrometry. Cancer Res, 64(24), 9018-26 (2004)

  • [46]K. Mikuriya, Y. Kuramitsu, S. Ryozawa, M. Fujimoto, S. Mori, M. Oka, K. Hamano, K. Okita, I. Sakaida and K. Nakamura: Expression of glycolytic enzymes is increased in pancreatic cancerous tissues as evidenced by proteomic profiling by two-dimensional electrophoresis and liquid chromatography-mass spectrometry/mass spectrometry. Int J Oncol, 30(4), 849-55 (2007)

  • [47]P. Cappello, B. Tomaino, R. Chiarle, P. Ceruti, A. Novarino, C. Castagnoli, P. Migliorini, G. Perconti, A. Giallongo, M. Milella, V. Monsurro, S. Barbi, A. Scarpa, P. Nistico, M. Giovarelli and F. Novelli: An integrated humoral and cellular response is elicited in pancreatic cancer by alpha-enolase, a novel pancreatic ductal adenocarcinoma-associated antigen. Int J Cancer, 125(3), 639-48 (2009)

  • [48]M. Principe, P. Ceruti, N. Y. Shih, M. S. Chattaragada, S. Rolla, L. Conti, M. Bestagno, L. Zentilin, S. H. Yang, P. Migliorini, P. Cappello, O. Burrone and F. Novelli: Targeting of surface alpha-enolase inhibits the invasiveness of pancreatic cancer cells. Oncotarget, 6(13), 11098-113 (2015)

  • [49]I. Rehman, A. R. Azzouzi, J. W. Catto, S. Allen, S. S. Cross, K. Feeley, M. Meuth and F. C. Hamdy: Proteomic analysis of voided urine after prostatic massage from patients with prostate cancer: a pilot study. Urology, 64(6), 1238-43 (2004)

  • [50]A. Suzuki, A. Iizuka, M. Komiyama, M. Takikawa, A. Kume, S. Tai, C. Ohshita, A. Kurusu, Y. Nakamura, A. Yamamoto, N. Yamazaki, S. Yoshikawa, Y. Kiyohara and Y. Akiyama: Identification of melanoma antigens using a Serological Proteome Approach (SERPA). Cancer Genomics Proteomics, 7(1), 17-23 (2010)

  • [51]R. Rucksaken, C. Pairojkul, P. Pinlaor, N. Khuntikeo, S. Roytrakul, C. Selmi and S. Pinlaor: Plasma autoantibodies against heat shock protein 70, enolase 1 and ribonuclease/angiogenin inhibitor 1 as potential biomarkers for cholangiocarcinoma. PLoS One, 9(7), e103259 (2014)

  • [52]Z. Mojtahedi, A. Safaei, Z. Yousefi and A. Ghaderi: Immunoproteomics of HER2-positive and HER2-negative breast cancer patients with positive lymph nodes. OMICS, 15(6), 409-18 (2011)

  • [53]S. Shukla, R. B. Govekar, R. Sirdeshmukh, C. S. Sundaram, A. K. D’Cruz, K. A. Pathak, S. V. Kane and S. M. Zingde: Tumor antigens eliciting autoantibody response in cancer of gingivo-buccal complex. Proteomics Clin Appl, 1(12), 1592-604 (2007)

  • [54]S. Shukla, A. Pranay, A. K. D’Cruz, P. Chaturvedi, S. V. Kane and S. M. Zingde: Immunoproteomics reveals that cancer of the tongue and the gingivobuccal complex exhibit differential autoantibody response. Cancer Biomark, 5(3), 127-35 (2009)

  • [55]J. W. Cui, W. H. Li, J. Wang, A. L. Li, H. Y. Li, H. X. Wang, K. He, W. Li, L. H. Kang, M. Yu, B. F. Shen, G. J. Wang and X. M. Zhang: Proteomics-based identification of human acute leukemia antigens that induce humoral immune response. Mol Cell Proteomics, 4(11), 1718-24 (2005)

  • [56]L. Zou, Y. Wu, L. Pei, D. Zhong, M. Gen, T. Zhao, J. Wu, B. Ni, Z. Mou, J. Han, Y. Chen and Y. Zhi: Identification of leukemia-associated antigens in chronic myeloid leukemia by proteomic analysis. Leuk Res, 29(12), 1387-91 (2005)

  • [57]B. Tomaino, P. Cappello, M. Capello, C. Fredolini, I. Sperduti, P. Migliorini, P. Salacone, A. Novarino, A. Giacobino, L. Ciuffreda, M. Alessio, P. Nistico, A. Scarpa, P. Pederzoli, W. Zhou, E. F. Petricoin Iii, L. A. Liotta, M. Giovarelli, M. Milella and F. Novelli: Circulating autoantibodies to phosphorylated alpha-enolase are a hallmark of pancreatic cancer. J Proteome Res, 10(1), 105-12 (2011)

  • [58]M. Forgber, U. Trefzer, W. Sterry and P. Walden: Proteome serological determination of tumor-associated antigens in melanoma. PLoS One, 4(4), e5199 (2009)

  • [59]P. He, T. Naka, S. Serada, M. Fujimoto, T. Tanaka, S. Hashimoto, Y. Shima, T. Yamadori, H. Suzuki, T. Hirashima, K. Matsui, H. Shiono, M. Okumura, T. Nishida, I. Tachibana, N. Norioka, S. Norioka and I. Kawase: Proteomics-based identification of alpha-enolase as a tumor antigen in non-small lung cancer. Cancer Sci, 98(8), 1234-40 (2007)

  • [60]R. Jankowska, D. Witkowska, I. Porebska, M. Kuropatwa, E. Kurowska and W. A. Gorczyca: Serum antibodies to retinal antigens in lung cancer and sarcoidosis. Pathobiology, 71(6), 323-8 (2004)

  • [61]K. Ueda: (Proteome analysis of autoantibodies in sera of patients with cancer). Rinsho Byori, 53(5), 437-45 (2005)

  • [62]T. Nakanishi, T. Takeuchi, K. Ueda, H. Murao and A. Shimizu: Detection of eight antibodies in cancer patients’ sera against proteins derived from the adenocarcinoma A549 cell line using proteomics-based analysis. J Chromatogr B Analyt Technol Biomed Life Sci, 838(1), 15-20 (2006)

  • [63]N. Y. Shih, H. L. Lai, G. C. Chang, H. C. Lin, Y. C. Wu, J. M. Liu, K. J. Liu and S. W. Tseng: Anti-alpha-enolase autoantibodies are down-regulated in advanced cancer patients. Jpn J Clin Oncol, 40(7), 663-9 (2010)

  • [64]K. C. Hsiao, N. Y. Shih, P. Y. Chu, Y. M. Hung, J. Y. Liao, S. W. Chou, Y. Y. Yang, G. C. Chang and K. J. Liu: Anti-alpha-enolase is a prognostic marker in postoperative lung cancer patients. Oncotarget, 6(33), 35073-86 (2015)

  • [65]P. L. Triozzi, W. Aldrich, J. W. Crabb and A. D. Singh: Spontaneous cellular and humoral tumor antigen responses in patients with uveal melanoma. Melanoma Res, 25(6), 510-8 (2015)

  • [66]M. Bruschi, R. A. Sinico, G. Moroni, F. Pratesi, P. Migliorini, M. Galetti, C. Murtas, A. Tincani, M. Madaio, A. Radice, F. Franceschini, B. Trezzi, L. Bianchi, A. Giallongo, R. Gatti, R. Tardanico, A. Scaloni, C. D’Ambrosio, M. L. Carnevali, P. Messa, P. Ravani, G. Barbano, B. Bianco, A. Bonanni, F. Scolari, A. Martini, G. Candiano, L. Allegri and G. M. Ghiggeri: Glomerular autoimmune multicomponents of human lupus nephritis In vivo: alpha-enolase and annexin AI. J Am Soc Nephrol, 25(11), 2483-98 (2014)

  • [67]M. Bruschi, M. Galetti, R. A. Sinico, G. Moroni, A. Bonanni, A. Radice, A. Tincani, F. Pratesi, P. Migliorini, C. Murtas, F. Franceschini, B. Trezzi, F. Brunini, R. Gatti, R. Tardanico, G. Barbano, G. Piaggio, P. Messa, P. Ravani, F. Scolari, G. Candiano, A. Martini, L. Allegri and G. M. Ghiggeri: Glomerular Autoimmune Multicomponents of Human Lupus Nephritis In vivo (2): Planted Antigens. J Am Soc Nephrol, 26(8), 1905-24 (2015)

  • [68]A. Magrys, T. Anekonda, G. Ren and G. Adamus: The role of anti-alpha-enolase autoantibodies in pathogenicity of autoimmune-mediated retinopathy. J Clin Immunol, 27(2), 181-92 (2007)

  • [69]G. Adamus, N. Aptsiauri, J. Guy, J. Heckenlively, J. Flannery and P. A. Hargrave: The occurrence of serum autoantibodies against enolase in cancer-associated retinopathy. Clin Immunol Immunopathol, 78(2), 120-9 (1996)

  • [70]C. Dot, J. Guigay and G. Adamus: Anti-alpha-enolase antibodies in cancer-associated retinopathy with small cell carcinoma of the lung. Am J Ophthalmol, 139(4), 746-7 (2005)

  • [71]M. Ejma, M. Misiuk-Hojlo, W. A. Gorczyca, R. Podemski, S. Szymaniec, M. Kuropatwa, J. Rogozinska-Szczepka and W. Bartnik: Antibodies to 46-kDa retinal antigen in a patient with breast carcinoma and cancer-associated retinopathy. Breast Cancer Res Treat, 110(2), 269-71 (2008)

  • [72]G. Adamus: Latest updates on antiretinal autoantibodies associated with vision loss and breast cancer. Invest Ophthalmol Vis Sci, 56(3), 1680-8 (2015)

  • [73]A. Kinloch, V. Tatzer, R. Wait, D. Peston, K. Lundberg, P. Donatien, D. Moyes, P. C. Taylor and P. J. Venables: Identification of citrullinated alpha-enolase as a candidate autoantigen in rheumatoid arthritis. Arthritis Res Ther, 7(6), R1421-9 (2005)

  • [74]K. Lundberg, A. Kinloch, B. A. Fisher, N. Wegner, R. Wait, P. Charles, T. R. Mikuls and P. J. Venables: Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum, 58(10), 3009-19 (2008)

  • [75]R. Bei, L. Masuelli, C. Palumbo, M. Modesti and A. Modesti: A common repertoire of autoantibodies is shared by cancer and autoimmune disease patients: Inflammation in their induction and impact on tumor growth. Cancer Lett, 281(1), 8-23 (2009)

  • [76]W. Zhou, M. Capello, C. Fredolini, L. Piemonti, L. A. Liotta, F. Novelli and E. F. Petricoin: Mass spectrometry analysis of the post-translational modifications of alpha-enolase from pancreatic ductal adenocarcinoma cells. J Proteome Res, 9(6), 2929-36 (2010)

  • [77]F. Mohammed, M. Cobbold, A. L. Zarling, M. Salim, G. A. Barrett-Wilt, J. Shabanowitz, D. F. Hunt, V. H. Engelhard and B. E. Willcox: Phosphorylation-dependent interaction between antigenic peptides and MHC class I: a molecular basis for the presentation of transformed self. Nat Immunol, 9(11), 1236-43 (2008)

  • [78]M. Capello, C. Caorsi, P. J. Bogantes Hernandez, E. Dametto, F. E. Bertinetto, P. Magistroni, S. Rendine, A. Amoroso and F. Novelli: Phosphorylated alpha-enolase induces autoantibodies in HLA-DR8 pancreatic cancer patients and triggers HLA-DR8 restricted T-cell activation. Immunol Lett, 167(1), 11-6 (2015)

  • [79]N. Sato, Y. Nabeta, H. Kondo, H. Sahara, Y. Hirohashi, K. Kashiwagi, T. Kanaseki, Y. Sato, S. Rong, I. Hirai, K. Kamiguchi, Y. Tamura, A. Matsuura, S. Takahashi, T. Torigoe and H. Ikeda: Human CD8 and CD4 T cell epitopes of epithelial cancer antigens. Cancer Chemother Pharmacol, 46 Suppl, S86-90 (2000)

  • [80]H. Kondo, H. Sahara, A. Miyazaki, Y. Nabeta, Y. Hirohashi, T. Kanaseki, A. Yamaguchi, N. Yamada, K. Hirayama, M. Suzuki, J. Hamuro, T. Torigoe, N. Takahashi, G. I. Kohama, H. Ikeda and N. Sato: Natural antigenic peptides from squamous cell carcinoma recognized by autologous HLA-DR8-restricted CD4+ T cells. Jpn J Cancer Res, 93(8), 917-24 (2002)

  • [81]P. Cappello, S. Rolla, R. Chiarle, M. Principe, F. Cavallo, G. Perconti, S. Feo, M. Giovarelli and F. Novelli: Vaccination with ENO1 DNA prolongs survival of genetically engineered mice with pancreatic cancer. Gastroenterology, 144(5), 1098-106 (2013)

  • [82]A. Amedei, E. Niccolai, M. Benagiano, C. Della Bella, F. Cianchi, P. Bechi, A. Taddei, L. Bencini, M. Farsi, P. Cappello, D. Prisco, F. Novelli and M. M. D’Elios: Ex vivo analysis of pancreatic cancer-infiltrating T lymphocytes reveals that ENO-specific Tregs accumulate in tumor tissue and inhibit Th1/Th17 effector cell functions. Cancer Immunol Immunother, 62(7), 1249-60 (2013)

  • [83]E. Niccolai, P. Cappello, A. Taddei, F. Ricci, M. M. D’Elios, M. Benagiano, P. Bechi, L. Bencini, M. N. Ringressi, A. Coratti, F. Cianchi, L. Bonello, P. F. Di Celle, D. Prisco, F. Novelli and A. Amedei: Peripheral ENO1-specific T cells mirror the intratumoral immune response and their presence is a potential prognostic factor for pancreatic adenocarcinoma. Int J Oncol (2016)

  • [84]E. Bettelli, Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner and V. K. Kuchroo: Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature, 441(7090), 235-8 (2006)

  • [85]D. C. Linehan and P. S. Goedegebuure: CD25+ CD4+ regulatory T-cells in cancer. Immunol Res, 32(1-3), 155-68 (2005)

  • [86]U. K. Liyanage, T. T. Moore, H. G. Joo, Y. Tanaka, V. Herrmann, G. Doherty, J. A. Drebin, S. M. Strasberg, T. J. Eberlein, P. S. Goedegebuure and D. C. Linehan: Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol, 169(5), 2756-61 (2002)

  • [87]K. Tjensvoll, O. Nordgard and R. Smaaland: Circulating tumor cells in pancreatic cancer patients: methods of detection and clinical implications. Int J Cancer, 134(1), 1-8 (2014)

  • [88]F. C. Bidard, F. Huguet, C. Louvet, L. Mineur, O. Bouche, B. Chibaudel, P. Artru, F. Desseigne, J. B. Bachet, C. Mathiot, J. Y. Pierga and P. Hammel: Circulating tumor cells in locally advanced pancreatic adenocarcinoma: the ancillary CirCe 07 study to the LAP 07 trial. Ann Oncol, 24(8), 2057-61 (2013)

  • [89]V. Pancholi: Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci, 58(7), 902-20 (2001)

  • [90]O. Warburg, F. Wind and E. Neglers: The metabolism of tumors. London: Constable & Co (1930)

  • [91]P. Ceruti, M. Principe, M. Capello, P. Cappello and F. Novelli: Three are better than one: plasminogen receptors as cancer theranostic targets. Exp Hematol Oncol, 2(1), 12 (2013)

  • [92]L. M. Phan, S. C. Yeung and M. H. Lee: Cancer metabolic reprogramming: importance, main features, and potentials for precise targeted anti-cancer therapies. Cancer Biol Med, 11(1), 1-19 (2014)

  • [93]O. Warburg, F. Wind and E. Negelein: The Metabolism of Tumors in the Body. J Gen Physiol, 8(6), 519-30 (1927)

  • [94]M. Capello, S. Ferri-Borgogno, C. Riganti, M. S. Chattaragada, M. Principe, C. Roux, W. Zhou, E. F. Petricoin, P. Cappello and F. Novelli: Targeting the Warburg effect in cancer cells through ENO1 knockdown rescues oxidative phosphorylation and induces growth arrest. Oncotarget, 7(5), 5598-612 (2016)

  • [95]M. Zhao, W. Fang, Y. Wang, S. Guo, L. Shu, L. Wang, Y. Chen, Q. Fu, Y. Liu, S. Hua, Y. Fan, X. Deng, R. Luo, Z. Mei, Q. Jiang and Z. Liu: Enolase-1 is a therapeutic target in endometrial carcinoma. Oncotarget, 6(17), 15610-27 (2015)

  • [96]E. Bobrovnikova-Marjon and J. B. Hurov: Targeting metabolic changes in cancer: novel therapeutic approaches. Annu Rev Med, 65, 157-70 (2014)

  • [97]M. Vander Heiden: Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov, 10(9), 671-84 (2011)

  • [98]L. Zhao, Y. Mao, Y. Zhao, Y. Cao and X. Chen: Role of multifaceted regulators in cancer glucose metabolism and their clinical significance. Oncotarget (2016)

  • [99]Y. Zhao, E. B. Butler and M. Tan: Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis, 4, e532 (2013)

  • [100]Y. Zhao, H. Liu, A. I. Riker, O. Fodstad, S. P. Ledoux, G. L. Wilson and M. Tan: Emerging metabolic targets in cancer therapy. Front Biosci (Landmark Ed), 16, 1844-60 (2011)

  • [101]H. Pelicano, D. S. Martin, R. H. Xu and P. Huang: Glycolysis inhibition for anticancer treatment. Oncogene, 25(34), 4633-46 (2006)

  • [102]A. K. Chan, J. Bruce and A. K. Siriwardena: Glucose metabolic phenotype of pancreatic cancer. World J Gastroenterol, 22(12), 3471-85 (2016)

  • [103]M. Sanzey, S. A. Abdul Rahim, A. Oudin, A. Dirkse, T. Kaoma, L. Vallar, C. Herold-Mende, R. Bjerkvig, A. Golebiewska and S. P. Niclou: Comprehensive analysis of glycolytic enzymes as therapeutic targets in the treatment of glioblastoma. PLoS One, 10(5), e0123544 (2015)

  • [104]R. Scatena, P. Bottoni, A. Pontoglio, L. Mastrototaro and B. Giardina: Glycolytic enzyme inhibitors in cancer treatment. Expert Opin Investig Drugs, 17(10), 1533-45 (2008)

  • [105]T. G. Spring and F. Wold: Studies on two high-affinity enolase inhibitors. Chemical characterization. Biochemistry, 10(25), 4649-54 (1971)

  • [106]A. S. N. M. V. de, S. M. Gomes Dias, L. V. Mello, M. T. da Silva Giotto, S. Gavalda, C. Blonski, R. C. Garratt and D. J. Rigden: Structural flexibility in Trypanosoma brucei enolase revealed by X-ray crystallography and molecular dynamics. Febs J, 274(19), 5077-89 (2007)

  • [107]F. L. Muller, S. Colla, E. Aquilanti, V. E. Manzo, G. Genovese, J. Lee, D. Eisenson, R. Narurkar, P. Deng, L. Nezi, M. A. Lee, B. Hu, J. Hu, E. Sahin, D. Ong, E. Fletcher-Sananikone, D. Ho, L. Kwong, C. Brennan, Y. A. Wang, L. Chin and R. A. DePinho: Passenger deletions generate therapeutic vulnerabilities in cancer. Nature, 488(7411), 337-42 (2012)

  • [108]D. W. Jung, W. H. Kim, S. H. Park, J. Lee, J. Kim, D. Su, H. H. Ha, Y. T. Chang and D. R. Williams: A unique small molecule inhibitor of enolase clarifies its role in fundamental biological processes. ACS Chem Biol, 8(6), 1271-82 (2013)

  • [109]X. Zhu, X. Miao, Y. Wu, C. Li, Y. Guo, Y. Liu, Y. Chen, X. Lu, Y. Wang and S. He: ENO1 promotes tumor proliferation and cell adhesion mediated drug resistance (CAM-DR) in Non-Hodgkin’s Lymphomas. Exp Cell Res, 335(2), 216-23 (2015)

  • [110]J. Gao, R. Zhao, Y. Xue, Z. Niu, K. Cui, F. Yu, B. Zhang and S. Li: Role of enolase-1 in response to hypoxia in breast cancer: exploring the mechanisms of action. Oncol Rep, 29(4), 1322-32 (2013)

  • [111]J. L. Walsh, T. J. Keith and H. R. Knull: Glycolytic enzyme interactions with tubulin and microtubules. Biochim Biophys Acta, 999(1), 64-70 (1989)

  • [112]K. Liu and N. Y. Shih: The role of Enolase in tissue invasion and metastasis of pathogens and tumor cells. J Cancer Mol, 3, 45–48 (2007)

  • [113]Q. F. Fu, Y. Liu, Y. Fan, S. N. Hua, H. Y. Qu, S. W. Dong, R. L. Li, M. Y. Zhao, Y. Zhen, X. L. Yu, Y. Y. Chen, R. C. Luo, R. Li, L. B. Li, X. J. Deng, W. Y. Fang, Z. Liu and X. Song: Alpha-enolase promotes cell glycolysis, growth, migration, and invasion in non-small cell lung cancer through FAK-mediated PI3K/AKT pathway. J Hematol Oncol, 8, 22 (2015)

  • [114]C. H. Wu, Y. H. Kuo, R. L. Hong and H. C. Wu: alpha-Enolase-binding peptide enhances drug delivery efficiency and therapeutic efficacy against colorectal cancer. Sci Transl Med, 7(290), 290ra91 (2015)

  • [115]I. Melero, S. Hervas-Stubbs, M. Glennie, D. M. Pardoll and L. Chen: Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer, 7(2), 95-106 (2007)

  • [116]P. E. Hughes, S. Caenepeel and L. C. Wu: Targeted Therapy and Checkpoint Immunotherapy Combinations for the Treatment of Cancer. Trends Immunol (2016)

  • [117]M. K. Callahan, M. A. Postow and J. D. Wolchok: Targeting T Cell Co-receptors for Cancer Therapy. Immunity, 44(5), 1069-78 (2016)

  • [118]D. N. Khalil, E. L. Smith, R. J. Brentjens and J. D. Wolchok: The future of cancer treatment: immunomodulation, CARs and combination immunotherapy. Nat Rev Clin Oncol, 13(6), 394 (2016)

  • [119]L. Vandenberk, J. Belmans, M. Van Woensel, M. Riva and S. W. Van Gool: Exploiting the Immunogenic Potential of Cancer Cells for Improved Dendritic Cell Vaccines. Front Immunol, 6, 663 (2015)

  • [120]F. Aranda, E. Vacchelli, A. Eggermont, J. Galon, C. Sautes-Fridman, E. Tartour, L. Zitvogel, G. Kroemer and L. Galluzzi: Trial Watch: Peptide vaccines in cancer therapy. Oncoimmunology, 2(12), e26621 (2013)

  • [121]J. Rice, C. H. Ottensmeier and F. K. Stevenson: DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer, 8(2), 108-20 (2008)

  • [122]L. M. Kranz, M. Diken, H. Haas, S. Kreiter, C. Loquai, K. C. Reuter, M. Meng, D. Fritz, F. Vascotto, H. Hefesha, C. Grunwitz, M. Vormehr, Y. Husemann, A. Selmi, A. N. Kuhn, J. Buck, E. Derhovanessian, R. Rae, S. Attig, J. Diekmann, R. A. Jabulowsky, S. Heesch, J. Hassel, P. Langguth, S. Grabbe, C. Huber, O. Tureci and U. Sahin: Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature (2016)

  • [123]J. Couzin-Frankel: Breakthrough of the year 2013. Cancer immunotherapy. Science, 342(6165), 1432-3 (2013)

  • [124]Z. Wang, P. J. Troilo, X. Wang, T. G. Griffiths, S. J. Pacchione, A. B. Barnum, L. B. Harper, C. J. Pauley, Z. Niu, L. Denisova, T. T. Follmer, G. Rizzuto, G. Ciliberto, E. Fattori, N. L. Monica, S. Manam and B. J. Ledwith: Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther, 11(8), 711-21 (2004)

  • [125]P. Cappello and F. Novelli: A self antigen reopens the games in pancreatic cancer. Oncoimmunology, 2(6), e24384 (2013)

  • [126]G. F. Castino, N. Cortese, G. Capretti, S. Serio, G. Di Caro, R. Mineri, E. Magrini, F. Grizzi, P. Cappello, F. Novelli, P. Spaggiari, M. Roncalli, C. Ridolfi, F. Gavazzi, A. Zerbi, P. Allavena and F. Marchesi: Spatial distribution of B cells predicts prognosis in human pancreatic adenocarcinoma. Oncoimmunology, 5(4), e1085147 (2016)

  • [127]P. Cappello, E. Tonoli, R. Curto, D. Giordano, M. Giovarelli and F. Novelli: Anti-α-enolase antibody limits the invasion of myeloid-derived suppressor cells and attenuates their restraining effector T cell response. Oncoimmunology, 5(5) (2016)

  • [128]E. Hirsch and F. Novelli: Cancer: natural-born killers unleashed. Nature, 510(7505), 342-3 (2014)

  • [129]K. Ali, D. R. Soond, R. Pineiro, T. Hagemann, W. Pearce, E. L. Lim, H. Bouabe, C. L. Scudamore, T. Hancox, H. Maecker, L. Friedman, M. Turner, K. Okkenhaug and B. Vanhaesebroeck: Inactivation of PI(3)K p110delta breaks regulatory T-cell-mediated immune tolerance to cancer. Nature, 510(7505), 407-11 (2014)

  • [130]M. M. Kaneda, P. Cappello, A. V. Nguyen, N. Ralainirina, C. R. Hardamon, P. Foubert, M. C. Schmid, P. Sun, E. Mose, M. Bouvet, A. M. Lowy, M. A. Valasek, R. Sasik, F. Novelli, E. Hirsch and J. A. Varner: Macrophage PI3Kgamma drives pancreatic ductal adenocarcinoma progression. Cancer Discov (2016)

Article Metrics

  • Information

  • Download

  • Contents

Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.

1 Jan 2017Review

Alpha-Enolase (ENO1), a potential target in novel immunotherapies

Paola Cappello 1,2,3, Moitza Principe 1,3, Sara Bulfamante 1,3, Francesco Novelli 1,2,3,4,*
Affiliations
Article Info

1 Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin, 10126 Italy

2 Molecular Biotechnology Center, University of Turin, Turin, 10126 Italy

3 Center for Experimental Research and Medical Studies, Turin, 10126 Italy

4 Immunogenetics and Transplantation Biology Service, Azienda Universitaria Ospedaliera Città Della Salute e Della Scienza di Torino, Torino 10126 Italy

Abstract

Alpha-enolase (ENO1) is a metabolic enzyme involved in the synthesis of pyruvate. It also acts as a plasminogen receptor and mediates the activation of plasmin and extracellular matrix degradation. In tumor cells, ENO1 is up-regulated and supports the Warburg effect; it is expressed at the cell surface, where it promotes cancer invasion, and is subjected to a specific array of post-translational modifications, namely acetylation, methylation and phosphorylation. ENO1 overexpression and post-translational modifications could be of diagnostic and prognostic value in many cancer types. Information on the biochemical, proteomics and immunological characterization of ENO1, and particularly its ability to trigger a strong specific humoral and cellular immune response, make this ubiquitous protein an interesting tumor target; DNA vaccination with ENO1 in preclinical models efficiently delays the development of very aggressive tumors such as pancreatic cancer. This review aims to analyze the main stages by which the tumor associated antigen (TAA) ENO1 has become a promising target that opens potential avenues for cancer im

Keywords

  • Alpha-enolase
  • ENO1
  • Cancer
  • Humoral Response
  • Glycolysis
  • Invasion
  • Immunotherapy
  • Pancreatic Cancer
  • Plasminogen Receptor
  • T cell response
  • Vaccination
  • TAAs
  • Metastasis
  • Review

References