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01-12-2013 | NON-THEMATIC REVIEW

The role of tumour-associated MUC1 in epithelial ovarian cancer metastasis and progression

Authors: Junli Deng, Li Wang, Hongmin Chen, Lei Li, Yiming Ma, Jie Ni, Yong Li

Published in: Cancer and Metastasis Reviews | Issue 3-4/2013

Abstract

The most common ovarian cancer is epithelial ovarian cancer (EOC) characterised by few early symptoms, widespread peritoneal dissemination and ascites at advanced stages that result in poor prognosis. Despite the recent progress in its management, including surgery and chemotherapy, EOC remains the most lethal gynaecological malignancy in women. Due to the limitations of current therapeutic approaches, many patients die of secondary disease (metastasis). MUC1 is associated with cellular transformation and tumorigenicity and is considered as an attractive therapeutic target for cancer therapy owning to its over-expression in most adenocarcinomas including EOC. Tumour-associated MUC1 plays an important role in EOC metastasis and progression. In neoplastic tissues, MUC1 is underglycosylated and reveals epitopes that are masked in the normal cells. This feature makes it possible to target tumour-associated MUC1 with antibodies, toxins or radionuclides or use a vaccine targeting tumour-associated MUC1 antigen. The shed tumour-associated MUC1 in blood can be used as a diagnostic biomarker for EOC detection and monitoring. Our recent results have shown that over-expression of MUC1 plays a very important role in EOC progression and MUC1 is an ideal target for targeted therapy to control metastatic and recurrent EOC. This review will summarize some important new findings supporting the role of MUC1 in EOC metastasis and progression and focus on the MUC1-based targeted therapy for control of metastatic and recurrent EOC.

Siegel, R., Naishadham, D., & Jemal, A. (2012). Cancer statistics, 2012. A Cancer Journal for Clinicians, 62, 10–29.CrossRef

Bhoola, S., & Hoskins, W. J. (2006). Diagnosis and management of epithelial ovarian cancer. Obstetrics and Gynecology, 107, 1399–1410.PubMedCrossRef

Yap, T. A., Carden, C. P., & Kaye, S. B. (2009). Beyond chemotherapy: targeted therapies in ovarian cancer. Nature Reviews. Cancer, 9, 167–181.PubMedCrossRef

Harries, M., & Kaye, S. B. (2001). Recent advances in the treatment of epithelial ovarian cancer. Expert Opinions on Investigational Drugs, 10, 1715–1724.CrossRef

Naora, H., & Montell, D. J. (2005). Ovarian cancer metastasis: integrating insights from disparate model organisms. Nature Reviews. Cancer, 5, 355–366.PubMedCrossRef

Balkwill, F., Bast, R. C., Berek, J., Chenevix-Trench, G., Gore, M., Hamilton, T., et al. (2003). Current research and treatment for epithelial ovarian cancer. A position paper from the Helene Harris Memorial Trust. European Journal of Cancer, 39, 1818–1827.PubMedCrossRef

Fleming, J. S., Beaugie, C. R., Haviv, I., Chenevix-Trench, G., & Tan, O. L. (2006). Incessant ovulation, inflammation and epithelial ovarian carcinogenesis: revisiting old hypotheses. Molecular and Cellular Endocrinology, 247, 4–21.PubMedCrossRef

Frederick, P. J., Straughn, J. M., Jr., Alvarez, R. D., & Buchsbaum, D. J. (2009). Preclinical studies and clinical utilization of monoclonal antibodies in epithelial ovarian cancer. Gynecological Oncology, 113, 384–390.CrossRef

Taylor-Papadimitriou, J., Burchell, J., Miles, D. W., & Dalziel, M. (1999). MUC1 and cancer. Biochimica et Biophysica Acta, 1455, 301–313.PubMedCrossRef

10.

Gendler, S. J. (2001). MUC1, the renaissance molecule. Journal of Mammary Gland Biological Neoplasia, 6, 339–353.CrossRef

11.

Rahn, J. J., Dabbagh, L., Pasdar, M., & Hugh, J. C. (2001). The importance of MUC1 cellular localization in patients with breast carcinoma: an immunohistologic study of 71 patients and review of the literature. Cancer, 91, 1973–1982.PubMedCrossRef

12.

Li, Y., Cozzi, P. J., & Russell, P. J. (2010). Promising tumor-associated antigens for future prostate cancer therapy. Medicinal Research Reviews, 30, 67–101.PubMed

13.

Hird, V., Maraveyas, A., Snook, D., Dhokia, B., Soutter, W. P., Meares, C., et al. (1993). Adjuvant therapy of ovarian cancer with radioactive monoclonal antibody. British Journal of Cancer, 68, 403–406.PubMedCrossRef

14.

Dong, Y., Walsh, M. D., Cummings, M. C., Wright, R. G., Khoo, S. K., Parsons, P. G., et al. (1997). Expression of MUC1 and MUC2 mucins in epithelial ovarian tumours. The Journal of Pathology, 183, 311–317.PubMedCrossRef

15.

Hu, X. F., Yang, E., Li, J., & Xing, P. X. (2006). MUC1 cytoplasmic tail: a potential therapeutic target for ovarian carcinoma. Expert Review of Anticancer Therapy, 6, 1261–1271.PubMedCrossRef

16.

Wang, L., Ma, J., Liu, F., Yu, Q., Chu, G., Perkins, A. C., et al. (2007). Expression of MUC1 in primary and metastatic human epithelial ovarian cancer and its therapeutic significance. Gynecological Oncology, 105, 695–702.CrossRef

17.

Van Elssen, C. H., Frings, P. W., Bot, F. J., Van de Vijver, K. K., Huls, M. B., Meek, B., et al. (2010). Expression of aberrantly glycosylated Mucin-1 in ovarian cancer. Histopathology, 57, 597–606.PubMedCrossRef

18.

Hollingsworth, M. A., & Swanson, B. J. (2004). Mucins in cancer: protection and control of the cell surface. Nature Reviews. Cancer, 4, 45–60.PubMedCrossRef

19.

Price, M. R., Hudecz, F., O’Sullivan, C., Baldwin, R. W., Edwards, P. M., & Tendler, S. J. (1990). Immunological and structural features of the protein core of human polymorphic epithelial mucin. Molecular Immunology, 27, 795–802.PubMedCrossRef

20.

Ligtenberg, M. J., Kruijshaar, L., Buijs, F., van Meijer, M., Litvinov, S. V., & Hilkens, J. (1992). Cell-associated episialin is a complex containing two proteins derived from a common precursor. The Journal of Biological Chemistry, 267, 6171–6177.PubMed

21.

Gendler, S. J., Burchell, J. M., Duhig, T., Lamport, D., White, R., Parker, M., et al. (1987). Cloning of partial cDNA encoding differentiation and tumor-associated mucin glycoproteins expressed by human mammary epithelium. Proceedings of the National Academy of Sciences of the United States of America, 84, 6060–6064.PubMedCrossRef

22.

Gendler, S. J., Lancaster, C. A., Taylor-Papadimitriou, J., Duhig, T., Peat, N., Burchell, J., et al. (1990). Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. The Journal of Biological Chemistry, 265, 15286–15293.PubMed

23.

Brockhausen, I., Yang, J. M., Burchell, J., Whitehouse, C., & Taylor-Papadimitriou, J. (1995). Mechanisms underlying aberrant glycosylation of MUC1 mucin in breast cancer cells. European journal of biochemistry / FEBS, 233, 607–617.PubMedCrossRef

24.

Burchell, J., Poulsom, R., Hanby, A., Whitehouse, C., Cooper, L., Clausen, H., et al. (1999). An alpha2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology, 9, 1307–1311.PubMedCrossRef

25.

Gendler, S. J., Spicer, A. P., Lalani, E. N., Duhig, T., Peat, N., Burchell, J., et al. (1991). Structure and biology of a carcinoma-associated mucin, MUC1. The American Review of Respiratory Disease, 144, S42–47.PubMedCrossRef

26.

Hanisch, F. G., Stadie, T. R., Deutzmann, F., & Peter-Katalinic, J. (1996). MUC1 glycoforms in breast cancer—cell line T47D as a model for carcinoma-associated alterations of O-glycosylation. European journal of biochemistry / FEBS, 236, 318–327.PubMedCrossRef

27.

Hanisch, F. G., & Muller, S. (2000). MUC1: the polymorphic appearance of a human mucin. Glycobiology, 10, 439–449.PubMedCrossRef

28.

Zrihan-Licht, S., Vos, H. L., Baruch, A., Elroy-Stein, O., Sagiv, D., Keydar, I., et al. (1994). Characterization and molecular cloning of a novel MUC1 protein, devoid of tandem repeats, expressed in human breast cancer tissue. European journal of biochemistry / FEBS, 224, 787–795.PubMedCrossRef

29.

Smorodinsky, N., Weiss, M., Hartmann, M. L., Baruch, A., Harness, E., Yaakobovitz, M., et al. (1996). Detection of a secreted MUC1/SEC protein by MUC1 isoform specific monoclonal antibodies. Biochemical and Biophysical Research Communications, 228, 115–121.PubMedCrossRef

30.

Oosterkamp, H. M., Scheiner, L., Stefanova, M. C., Lloyd, K. O., & Finstad, C. L. (1997). Comparison of MUC-1 mucin expression in epithelial and non-epithelial cancer cell lines and demonstration of a new short variant form (MUC-1/Z). International journal of cancer. Journal international du cancer, 72, 87–94.PubMedCrossRef

31.

Baruch, A., Hartmann, M., Yoeli, M., Adereth, Y., Greenstein, S., Stadler, Y., et al. (1999). The breast cancer-associated MUC1 gene generates both a receptor and its cognate binding protein. Cancer Research, 59, 1552–1561.PubMed

32.

Baruch, A., Hartmann, M., Zrihan-Licht, S., Greenstein, S., Burstein, M., Keydar, I., et al. (1997). Preferential expression of novel MUC1 tumor antigen isoforms in human epithelial tumors and their tumor-potentiating function. International journal of cancer. Journal international du cancer, 71, 741–749.PubMedCrossRef

33.

Spicer, A. P., Duhig, T., Chilton, B. S., & Gendler, S. J. (1995). Analysis of mammalian MUC1 genes reveals potential functionally important domains. Mammalian genome: official journal of the International Mammalian Genome Society, 6, 885–888.CrossRef

34.

Singh, P. K., & Hollingsworth, M. A. (2006). Cell surface-associated mucins in signal transduction. Trends in Cell Biology, 16, 467–476.PubMedCrossRef

35.

Hattrup, C. L., & Gendler, S. J. (2008). Structure and function of the cell surface (tethered) mucins. Annual Review of Physiology, 70, 431–457.PubMedCrossRef

36.

Kohlgraf, K. G., Gawron, A. J., Higashi, M., Meza, J. L., Burdick, M. D., Kitajima, S., et al. (2003). Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line. Cancer Research, 63, 5011–5020.PubMed

37.

Mommers, E. C., Leonhart, A. M., von Mensdorff-Pouilly, S., Schol, D. J., Hilgers, J., Meijer, C. J., et al. (1999). Aberrant expression of MUC1 mucin in ductal hyperplasia and ductal carcinoma in situ of the breast. International journal of cancer. Journal international du cancer, 84, 466–469.PubMedCrossRef

38.

Gaemers, I. C., Vos, H. L., Volders, H. H., van der Valk, S. W., & Hilkens, J. (2001). A stat-responsive element in the promoter of the episialin/MUC1 gene is involved in its overexpression in carcinoma cells. The Journal of Biological Chemistry, 276, 6191–6199.PubMedCrossRef

39.

Wesseling, J., van der Valk, S. W., Vos, H. L., Sonnenberg, A., & Hilkens, J. (1995). Episialin (MUC1) overexpression inhibits integrin-mediated cell adhesion to extracellular matrix components. The Journal of Cell Biology, 129, 255–265.PubMedCrossRef

40.

Feng, H., Ghazizadeh, M., Konishi, H., & Araki, T. (2002). Expression of MUC1 and MUC2 mucin gene products in human ovarian carcinomas. Japanese Journal of Clinical Oncology, 32, 525–529.PubMedCrossRef

41.

McDermott, K. M., Crocker, P. R., Harris, A., Burdick, M. D., Hinoda, Y., Hayashi, T., et al. (2001). Overexpression of MUC1 reconfigures the binding properties of tumor cells. International journal of cancer. Journal international du cancer, 94, 783–791.PubMedCrossRef

42.

Zhang, K., Baeckstrom, D., Brevinge, H., & Hansson, G. C. (1996). Secreted MUC1 mucins lacking their cytoplasmic part and carrying sialyl-Lewis a and x epitopes from a tumor cell line and sera of colon carcinoma patients can inhibit HL-60 leukocyte adhesion to E-selectin-expressing endothelial cells. Journal of Cell Biochemistry, 60, 538–549.CrossRef

43.

Brinkman-Van der Linden, E. C., & Varki, A. (2000). New aspects of siglec binding specificities, including the significance of fucosylation and of the sialyl-Tn epitope. Sialic acid-binding immunoglobulin superfamily lectins. The Journal of Biological Chemistry, 275, 8625–8632.PubMedCrossRef

44.

Budiu, R.A., Elishaev, E., Brozick, J., Lee, M., Edwards, R.P., Kalinski, P., et al. (2012). Immunobiology of human mucin 1 in a preclinical ovarian tumor model. Oncogene. doi:10.1038/onc.2012.397.

45.

Karsten, U., von Mensdorff-Pouilly, S., & Goletz, S. (2005). What makes MUC1 a tumor antigen? Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine, 26, 217–220.CrossRef

46.

van de Wiel-van Kemenade, E., Ligtenberg, M. J., de Boer, A. J., Buijs, F., Vos, H. L., Melief, C. J., et al. (1993). Episialin (MUC1) inhibits cytotoxic lymphocyte-target cell interaction. Journal of Immunology, 151, 767–776.

47.

Hughes, O. D., Bishop, M. C., Perkins, A. C., Wastie, M. L., Denton, G., Price, M. R., et al. (2000). Targeting superficial bladder cancer by the intravesical administration of copper-67-labeled anti-MUC1 mucin monoclonal antibody C595. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 18, 363–370.

48.

Curiel, T. J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., et al. (2004). Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nature Medicine, 10, 942–949.PubMedCrossRef

49.

Sato, E., Olson, S. H., Ahn, J., Bundy, B., Nishikawa, H., Qian, F., et al. (2005). Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proceedings of the National Academy of Sciences of the United States of America, 102, 18538–18543.PubMedCrossRef

50.

Kryczek, I., Wei, S., Zhu, G., Myers, L., Mottram, P., Cheng, P., et al. (2007). Relationship between B7-H4, regulatory T cells, and patient outcome in human ovarian carcinoma. Cancer Research, 67, 8900–8905.PubMedCrossRef

51.

Ren, J., Agata, N., Chen, D., Li, Y., Yu, W. H., Huang, L., et al. (2004). Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell, 5, 163–175.PubMedCrossRef

52.

Wei, X., Xu, H., & Kufe, D. (2005). Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer Cell, 7, 167–178.PubMedCrossRef

53.

Yin, L., Huang, L., & Kufe, D. (2004). MUC1 oncoprotein activates the FOXO3a transcription factor in a survival response to oxidative stress. The Journal of Biological Chemistry, 279, 45721–45727.PubMedCrossRef

54.

Kalra, A. V., & Campbell, R. B. (2007). Mucin impedes cytotoxic effect of 5-FU against growth of human pancreatic cancer cells: overcoming cellular barriers for therapeutic gain. British Journal of Cancer, 97, 910–918.PubMedCrossRef

55.

Kalra, A. V., & Campbell, R. B. (2009). Mucin overexpression limits the effectiveness of 5-FU by reducing intracellular drug uptake and antineoplastic drug effects in pancreatic tumours. European Journal of Cancer, 45, 164–173.PubMedCrossRef

56.

Hait, W. N., Jin, S., & Yang, J. M. (2006). A matter of life or death (or both): understanding autophagy in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research, 12, 1961–1965.CrossRef

57.

Peracchio, C., Alabiso, O., Valente, G., & Isidoro, C. (2012). Involvement of autophagy in ovarian cancer: a working hypothesis. Journal of Ovarian Research, 5, 22.PubMedCrossRef

58.

Amaravadi, R. K. (2008). Autophagy-induced tumor dormancy in ovarian cancer. Journal of Clinical Investigation, 118, 3837–3840.PubMed

59.

Yin, L., Kharbanda, S., & Kufe, D. (2009). MUC1 oncoprotein promotes autophagy in a survival response to glucose deprivation. International Journal of Oncology, 34, 1691–1699.PubMed

60.

Polyak, K., & Weinberg, R. A. (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature Reviews. Cancer, 9, 265–273.PubMedCrossRef

61.

Vergara, D., Merlot, B., Lucot, J. P., Collinet, P., Vinatier, D., Fournier, I., et al. (2010). Epithelial–mesenchymal transition in ovarian cancer. Cancer Letters, 291, 59–66.PubMedCrossRef

62.

Roy, L. D., Sahraei, M., Subramani, D. B., Besmer, D., Nath, S., Tinder, T. L., et al. (2011). MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene, 30, 1449–1459.PubMedCrossRef

63.

Rajabi, H., Ahmad, R., Jin, C., Joshi, M. D., Guha, M., Alam, M., et al. (2012). MUC1-C oncoprotein confers androgen-independent growth of human prostate cancer cells. Prostate, 72, 1659–1668.PubMedCrossRef

64.

Ahmed, N., Abubaker, K., Findlay, J., & Quinn, M. (2010). Epithelial mesenchymal transition and cancer stem cell-like phenotypes facilitate chemoresistance in recurrent ovarian cancer. Current Cancer Drug Targets, 10, 268–278.PubMedCrossRef

65.

Davidson, B., Trope, C. G., & Reich, R. (2012). Epithelial–mesenchymal transition in ovarian carcinoma. Front Oncology, 2, 33.

66.

Carraway, K. L., 3rd, Funes, M., Workman, H. C., & Sweeney, C. (2007). Contribution of membrane mucins to tumor progression through modulation of cellular growth signaling pathways. Current Topics in Developmental Biology, 78, 1–22.PubMedCrossRef

67.

Yamamoto, M., Bharti, A., Li, Y., & Kufe, D. (1997). Interaction of the DF3/MUC1 breast carcinoma-associated antigen and beta-catenin in cell adhesion. The Journal of Biological Chemistry, 272, 12492–12494.PubMedCrossRef

68.

Schroeder, J. A., Adriance, M. C., Thompson, M. C., Camenisch, T. D., & Gendler, S. J. (2003). MUC1 alters beta-catenin-dependent tumor formation and promotes cellular invasion. Oncogene, 22, 1324–1332.PubMedCrossRef

69.

Li, Y., Kuwahara, H., Ren, J., Wen, G., & Kufe, D. (2001). The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin. The Journal of Biological Chemistry, 276, 6061–6064.PubMedCrossRef

70.

Li, Y., Ren, J., Yu, W., Li, Q., Kuwahara, H., Yin, L., et al. (2001). The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and beta-catenin. The Journal of Biological Chemistry, 276, 35239–35242.PubMedCrossRef

71.

Li, Y., & Kufe, D. (2001). The Human DF3/MUC1 carcinoma-associated antigen signals nuclear localization of the catenin p120(ctn). Biochemical and Biophysical Research Communications, 281, 440–443.PubMedCrossRef

72.

Ren, J., Li, Y., & Kufe, D. (2002). Protein kinase C delta regulates function of the DF3/MUC1 carcinoma antigen in beta-catenin signaling. The Journal of Biological Chemistry, 277, 17616–17622.PubMedCrossRef

73.

Schroeder, J. A., Thompson, M. C., Gardner, M. M., & Gendler, S. J. (2001). Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. The Journal of Biological Chemistry, 276, 13057–13064.PubMedCrossRef

74.

Li, Y., Yu, W. H., Ren, J., Chen, W., Huang, L., Kharbanda, S., et al. (2003). Heregulin targets gamma-catenin to the nucleolus by a mechanism dependent on the DF3/MUC1 oncoprotein. Molecular Cancer Research, 1, 765–775.PubMed

75.

Pochampalli, M. R., el Bejjani, R. M., & Schroeder, J. A. (2007). MUC1 is a novel regulator of ErbB1 receptor trafficking. Oncogene, 26, 1693–1701.PubMedCrossRef

76.

Roepstorff, K., Grovdal, L., Grandal, M., Lerdrup, M., & van Deurs, B. (2008). Endocytic downregulation of ErbB receptors: mechanisms and relevance in cancer. Histochemistry and Cell Biology, 129, 563–578.PubMedCrossRef

77.

Hattrup, C. L., & Gendler, S. J. (2006). MUC1 alters oncogenic events and transcription in human breast cancer cells. Breast Cancer Research, 8, R37.PubMedCrossRef

78.

Pochampalli, M. R., Bitler, B. G., & Schroeder, J. A. (2007). Transforming growth factor alpha dependent cancer progression is modulated by Muc1. Cancer Research, 67, 6591–6598.PubMedCrossRef

79.

Bitler, B. G., Goverdhan, A., & Schroeder, J. A. (2010). MUC1 regulates nuclear localization and function of the epidermal growth factor receptor. Journal of Cell Science, 123, 1716–1723.PubMedCrossRef

80.

Bienz, M. (2005). beta-Catenin: a pivot between cell adhesion and Wnt signalling. Current Biology, 15, R64–67.PubMedCrossRef

81.

Moon, R. T., Kohn, A. D., De Ferrari, G. V., & Kaykas, A. (2004). WNT and beta-catenin signalling: diseases and therapies. Nature Reviews Genetics, 5, 691–701.PubMedCrossRef

82.

Hulsken, J., Behrens, J., & Birchmeier, W. (1994). Tumor-suppressor gene products in cell contacts: the cadherin-APC-armadillo connection. Current Opinion in Cell Biology, 6, 711–716.PubMedCrossRef

83.

Wen, Y., Caffrey, T. C., Wheelock, M. J., Johnson, K. R., & Hollingsworth, M. A. (2003). Nuclear association of the cytoplasmic tail of MUC1 and beta-catenin. The Journal of Biological Chemistry, 278, 38029–38039.PubMedCrossRef

84.

Huang, L., Chen, D., Liu, D., Yin, L., Kharbanda, S., & Kufe, D. (2005). MUC1 oncoprotein blocks glycogen synthase kinase 3beta-mediated phosphorylation and degradation of beta-catenin. Cancer Research, 65, 10413–10422.PubMedCrossRef

85.

Li, Y., Liu, D., Chen, D., Kharbanda, S., & Kufe, D. (2003). Human DF3/MUC1 carcinoma-associated protein functions as an oncogene. Oncogene, 22, 6107–6110.PubMedCrossRef

86.

Li, Y., Bharti, A., Chen, D., Gong, J., & Kufe, D. (1998). Interaction of glycogen synthase kinase 3beta with the DF3/MUC1 carcinoma-associated antigen and beta-catenin. Molecular and Cellular Biology, 18, 7216–7224.PubMed

87.

Havrilesky, L. J., Whitehead, C. M., Rubatt, J. M., Cheek, R. L., Groelke, J., He, Q., et al. (2008). Evaluation of biomarker panels for early stage ovarian cancer detection and monitoring for disease recurrence. Gynecologic Oncology, 110, 374–382.PubMedCrossRef

88.

Rein, B. J., Gupta, S., Dada, R., Safi, J., Michener, C., & Agarwal, A. (2011). Potential markers for detection and monitoring of ovarian cancer. Journal of Oncology, 2011, 475983.PubMedCrossRef

89.

Moore, L. E., Pfeiffer, R. M., Zhang, Z., Lu, K. H., Fung, E. T., & Bast, R. C., Jr. (2012). Proteomic biomarkers in combination with CA 125 for detection of epithelial ovarian cancer using prediagnostic serum samples from the Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial. Cancer, 118, 91–100.PubMedCrossRef

90.

Cannistra, S. A. (2004). Cancer of the ovary. The New England Journal of Medicine, 351, 2519–2529.PubMedCrossRef

91.

Fisken, J., Leonard, R. C., Badley, A., Jonrup, I., Aspinall, L., Sturgeon, C., et al. (1991). Serological monitoring of epithelial ovarian cancer. Disease Markers, 9, 175–190.PubMed

92.

Vuento, M. H., Stenman, U. H., Pirhonen, J. P., Makinen, J. I., Laippala, P. J., & Salmi, T. A. (1997). Significance of a single CA 125 assay combined with ultrasound in the early detection of ovarian and endometrial cancer. Gynecological Oncology, 64, 141–146.CrossRef

93.

Moore, R. G., & Maclaughlan, S. (2010). Current clinical use of biomarkers for epithelial ovarian cancer. Current Opinion in Oncology, 22, 492–497.PubMedCrossRef

94.

Fritz-Rdzanek, A., Grzybowski, W., Beta, J., Durczynski, A., & Jakimiuk, A. (2012). HE4 protein and SMRP: potential novel biomarkers in ovarian cancer detection. Oncology Letters, 4, 385–389.PubMed

95.

Baldus, S. E., Engelmann, K., & Hanisch, F. G. (2004). MUC1 and the MUCs: a family of human mucins with impact in cancer biology. Critical Reviews in Clinical Laboratory Sciences, 41, 189–231.PubMedCrossRef

96.

Sekine, H., Hayes, D. F., Ohno, T., Keefe, K. A., Schaetzl, E., Bast, R. C., et al. (1985). Circulating DF3 and CA125 antigen levels in serum from patients with epithelial ovarian carcinoma. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 3, 1355–1363.

97.

Bast, R. C., Jr., Feeney, M., Lazarus, H., Nadler, L. M., Colvin, R. B., & Knapp, R. C. (1981). Reactivity of a monoclonal antibody with human ovarian carcinoma. Journal of Clinical Investigation, 68, 1331–1337.PubMedCrossRef

98.

Fisken, J., Roulston, J. E., Sturgeon, C., Badley, R. A., Jonrup, I., Aspinall, L., et al. (1993). The value of the human milk fat globule membrane antigen HMFG2 in epithelial ovarian cancer monitoring: comparison with CA125. British Journal of Cancer, 67, 1065–1070.PubMedCrossRef

99.

Richards, E. R., Devine, P. L., Quin, R. J., Fontenot, J. D., Ward, B. G., & McGuckin, M. A. (1998). Antibodies reactive with the protein core of MUC1 mucin are present in ovarian cancer patients and healthy women. Cancer immunology, immunotherapy: CII, 46, 245–252.CrossRef

100.

Wandall, H. H., Blixt, O., Tarp, M. A., Pedersen, J. W., Bennett, E. P., Mandel, U., et al. (2010). Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Research, 70, 1306–1313.PubMedCrossRef

101.

Budiu, R. A., Mantia-Smaldone, G., Elishaev, E., Chu, T., Thaller, J., McCabe, K., et al. (2011). Soluble MUC1 and serum MUC1-specific antibodies are potential prognostic biomarkers for platinum-resistant ovarian cancer. Cancer immunology, immunotherapy: CII, 60, 975–984.CrossRef

102.

Danielczyk, A., Stahn, R., Faulstich, D., Loffler, A., Marten, A., Karsten, U., et al. (2006). PankoMab: a potent new generation anti-tumour MUC1 antibody. Cancer immunology, immunotherapy: CII, 55, 1337–1347.CrossRef

103.

Karsten, U., Diotel, C., Klich, G., Paulsen, H., Goletz, S., Muller, S., et al. (1998). Enhanced binding of antibodies to the DTR motif of MUC1 tandem repeat peptide is mediated by site-specific glycosylation. Cancer Research, 58, 2541–2549.PubMed

104.

Jeschke, U., Wiest, I., Schumacher, A. L., Kupka, M., Rack, B., Stahn, R., et al. (2012). Determination of MUC1 in sera of ovarian cancer patients and in sera of patients with benign changes of the ovaries with CA15-3, CA27.29, and PankoMab. Anticancer Research, 32, 2185–2189.PubMed

105.

Croghan, G. A., Wingate, M. B., Gamarra, M., Johnson, E., Chu, T. M., Allen, H., et al. (1984). Reactivity of monoclonal antibody F36/22 with human ovarian adenocarcinomas. Cancer Research, 44, 1954–1962.PubMed

106.

Friedman, E. L., Hayes, D. F., & Kufe, D. W. (1986). Reactivity of monoclonal antibody DF3 with a high molecular weight antigen expressed in human ovarian carcinomas. Cancer Research, 46, 5189–5194.PubMed

107.

Ward, B. G., Lowe, D. G., & Shepherd, J. H. (1987). Patterns of expression of a tumor associated antigen, defined by the monoclonal antibody HMFG2, in human epithelial ovarian carcinoma. Comparison with expression of the HMFG1, AUA1 and F36/22 antigens. Cancer, 60, 787–793.PubMedCrossRef

108.

Ichige, K., Perey, L., Vogel, C. A., Buchegger, F., & Kufe, D. (1995). Expression of the DF3-P epitope in human ovarian carcinomas. Clinical cancer research: an official journal of the American Association for Cancer Research, 1, 565–571.

109.

Drapkin, R., Crum, C. P., & Hecht, J. L. (2004). Expression of candidate tumor markers in ovarian carcinoma and benign ovary: evidence for a link between epithelial phenotype and neoplasia. Human Pathology, 35, 1014–1021.PubMedCrossRef

110.

Lau, S. K., Weiss, L. M., & Chu, P. G. (2004). Differential expression of MUC1, MUC2, and MUC5AC in carcinomas of various sites: an immunohistochemical study. American Journal of Clinical Pathology, 122, 61–69.PubMedCrossRef

111.

Tornos, C., Soslow, R., Chen, S., Akram, M., Hummer, A. J., Abu-Rustum, N., et al. (2005). Expression of WT1, CA 125, and GCDFP-15 as useful markers in the differential diagnosis of primary ovarian carcinomas versus metastatic breast cancer to the ovary. The American Journal of Surgical Pathology, 29, 1482–1489.PubMedCrossRef

112.

Lu, K. H., Patterson, A. P., Wang, L., Marquez, R. T., Atkinson, E. N., Baggerly, K. A., et al. (2004). Selection of potential markers for epithelial ovarian cancer with gene expression arrays and recursive descent partition analysis. Clinical cancer research: an official journal of the American Association for Cancer Research, 10, 3291–3300.CrossRef

113.

Rosen, D. G., Wang, L., Atkinson, J. N., Yu, Y., Lu, K. H., Diamandis, E. P., et al. (2005). Potential markers that complement expression of CA125 in epithelial ovarian cancer. Gynecological Oncology, 99, 267–277.CrossRef

114.

Takano, M., Fujii, K., Kita, T., Kikuchi, Y., & Uchida, K. (2004). Amplicon profiling reveals cytoplasmic overexpression of MUC1 protein as an indicator of resistance to platinum-based chemotherapy in patients with ovarian cancer. Oncology Reports, 12, 1177–1182.PubMed

115.

Tamada, Y., Takeuchi, H., Suzuki, N., Susumu, N., Aoki, D., & Irimura, T. (2007). Biological and therapeutic significance of MUC1 with sialoglycans in clear cell adenocarcinoma of the ovary. Cancer Science, 98, 1586–1591.PubMedCrossRef

116.

Cheever, M. A., Allison, J. P., Ferris, A. S., Finn, O. J., Hastings, B. M., Hecht, T. T., et al. (2009). The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clinical cancer research: an official journal of the American Association for Cancer Research, 15, 5323–5337.CrossRef

117.

Mabuchi, S., & Kimura, T. (2010). Treatment of ovarian cancer by monoclonal antibodies. Discovery Medicine, 9, 197–203.PubMed

118.

Mabuchi, S., Morishige, K., & Kimura, T. (2010). Use of monoclonal antibodies in the treatment of ovarian cancer. Current Opinion in Obstetrics and Gynecology, 22, 3–8.PubMedCrossRef

119.

Perkins, A. C., Symonds, I. M., Pimm, M. V., Price, M. R., Wastie, M. L., & Symonds, E. M. (1993). Immunoscintigraphy of ovarian carcinoma using a monoclonal antibody (111In-NCRC48) defining a polymorphic epithelial mucin (PEM) epitope. Nuclear Medicine Communications, 14, 578–586.PubMedCrossRef

120.

Song, Y. J., Qu, C. F., Rizvi, S. M., Li, Y., Robertson, G., Raja, C., et al. (2006). Cytotoxicity of PAI2, C595 and herceptin vectors labeled with the alpha-emitting radioisotope Bismuth-213 for ovarian cancer cell monolayers and clusters. Cancer Letters, 234, 176–183.PubMedCrossRef

121.

Song, E. Y., Qu, C. F., Rizvi, S. M., Raja, C., Beretov, J., Morgenstern, A., et al. (2008). Bismuth-213 radioimmunotherapy with C595 anti-MUC1 monoclonal antibody in an ovarian cancer ascites model. Cancer Biology & Therapy, 7, 76–80.CrossRef

122.

Wang, L., Chen, H., Liu, F., Madigan, M. C., Power, C. A., Hao, J., et al. (2011). Monoclonal antibody targeting MUC1 and increasing sensitivity to docetaxel as a novel strategy in treating human epithelial ovarian cancer. Cancer Letters, 300, 122–133.PubMedCrossRef

123.

Wang, L., Chen, H., Pourgholami, M. H., Beretov, J., Hao, J., Chao, H., et al. (2011). Anti-MUC1 monoclonal antibody (C595) and docetaxel markedly reduce tumor burden and ascites, and prolong survival in an in vivo ovarian cancer model. PLoS One, 6, e24405.PubMedCrossRef

124.

Nicholson, S., Bomphray, C. C., Thomas, H., McIndoe, A., Barton, D., Gore, M., et al. (2004). A phase I trial of idiotypic vaccination with HMFG1 in ovarian cancer. Cancer immunology, immunotherapy: CII, 53, 809–816.CrossRef

125.

Epenetos, A. A., Britton, K. E., Mather, S., Shepherd, J., Granowska, M., Taylor-Papadimitriou, J., et al. (1982). Targeting of iodine-123-labelled tumour-associated monoclonal antibodies to ovarian, breast, and gastrointestinal tumours. Lancet, 2, 999–1005.PubMedCrossRef

126.

Janssen, M. L., Pels, W., Massuger, L. F., Oyen, W. J., Boonstra, H., Corstens, F. H., et al. (2003). Intraperitoneal radioimmunotherapy in an ovarian carcinoma mouse model: effect of the radionuclide. International Journal of Gynecological Cancer, 13, 607–613.PubMedCrossRef

127.

Stewart, J. S., Hird, V., Snook, D., Dhokia, B., Sivolapenko, G., Hooker, G., et al. (1990). Intraperitoneal yttrium-90-labeled monoclonal antibody in ovarian cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 8, 1941–1950.

128.

Epenetos, A. A., Hird, V., Lambert, H., Mason, P., & Coulter, C. (2000). Long term survival of patients with advanced ovarian cancer treated with intraperitoneal radioimmunotherapy. International Journal of Gynecological Cancer, 10, 44–46.PubMedCrossRef

129.

Verheijen, R. H., Massuger, L. F., Benigno, B. B., Epenetos, A. A., Lopes, A., Soper, J. T., et al. (2006). Phase III trial of intraperitoneal therapy with yttrium-90-labeled HMFG1 murine monoclonal antibody in patients with epithelial ovarian cancer after a surgically defined complete remission. Journal of clinical oncology: official journal of the American Society of Clinical Oncology, 24, 571–578.CrossRef

130.

Oei, A. L., Verheijen, R. H., Seiden, M. V., Benigno, B. B., Lopes, A., Soper, J. T., et al. (2007). Decreased intraperitoneal disease recurrence in epithelial ovarian cancer patients receiving intraperitoneal consolidation treatment with yttrium-90-labeled murine HMFG1 without improvement in overall survival. International journal of cancer. Journal international du cancer, 120, 2710–2714.PubMedCrossRef

131.

Brossart, P., Wirths, S., Stuhler, G., Reichardt, V. L., Kanz, L., & Brugger, W. (2000). Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood, 96, 3102–3108.PubMed

132.

Holmberg, L. A., Oparin, D. V., Gooley, T., & Sandmaier, B. M. (2003). The role of cancer vaccines following autologous stem cell rescue in breast and ovarian cancer patients: experience with the STn-KLH vaccine (Theratope). Clinical Breast Cancer, 3(Suppl 4), S144–151.PubMedCrossRef

133.

Vlad, A. M., Kettel, J. C., Alajez, N. M., Carlos, C. A., & Finn, O. J. (2004). MUC1 immunobiology: from discovery to clinical applications. Advances in Immunology, 82, 249–293.PubMedCrossRef

134.

Sabbatini, P. J., Ragupathi, G., Hood, C., Aghajanian, C. A., Juretzka, M., Iasonos, A., et al. (2007). Pilot study of a heptavalent vaccine-keyhole limpet hemocyanin conjugate plus QS21 in patients with epithelial ovarian, fallopian tube, or peritoneal cancer. Clinical cancer research: an official journal of the American Association for Cancer Research, 13, 4170–4177.CrossRef

135.

Oei, A. L., Sweep, F. C., Thomas, C. M., Boerman, O. C., & Massuger, L. F. (2008). The use of monoclonal antibodies for the treatment of epithelial ovarian cancer (review). International Journal of Oncology, 32, 1145–1157.PubMedCrossRef

136.

Raina, D., Ahmad, R., Joshi, M. D., Yin, L., Wu, Z., Kawano, T., et al. (2009). Direct targeting of the mucin 1 oncoprotein blocks survival and tumorigenicity of human breast carcinoma cells. Cancer Research, 69, 5133–5141.PubMedCrossRef

137.

Bitler, B. G., Menzl, I., Huerta, C. L., Sands, B., Knowlton, W., Chang, A., et al. (2009). Intracellular MUC1 peptides inhibit cancer progression. Clinical cancer research: an official journal of the American Association for Cancer Research, 15, 100–109.CrossRef

138.

Osborne, S. E., Matsumura, I., & Ellington, A. D. (1997). Aptamers as therapeutic and diagnostic reagents: problems and prospects. Current Opinion in Chemical Biology, 1, 5–9.PubMedCrossRef

139.

Farokhzad, O. C., Jon, S., Khademhosseini, A., Tran, T. N., Lavan, D. A., & Langer, R. (2004). Nanoparticle–aptamer bioconjugates: a new approach for targeting prostate cancer cells. Cancer Research, 64, 7668–7672.PubMedCrossRef

140.

Huang, Y. F., Shangguan, D., Liu, H., Phillips, J. A., Zhang, X., Chen, Y., et al. (2009). Molecular assembly of an aptamer–drug conjugate for targeted drug delivery to tumor cells. Chembiochemistry, 10, 862–868.CrossRef

141.

Ferreira, C. S., Matthews, C. S., & Missailidis, S. (2006). DNA aptamers that bind to MUC1 tumour marker: design and characterization of MUC1-binding single-stranded DNA aptamers. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine, 27, 289–301.CrossRef

142.

Ferreira, C. S., Cheung, M. C., Missailidis, S., Bisland, S., & Gariepy, J. (2009). Phototoxic aptamers selectively enter and kill epithelial cancer cells. Nucleic Acids Research, 37, 866–876.PubMedCrossRef

143.

Savla, R., Taratula, O., Garbuzenko, O., & Minko, T. (2011). Tumor targeted quantum dot-mucin 1 aptamer-doxorubicin conjugate for imaging and treatment of cancer. Journal of controlled release: official journal of the Controlled Release Society, 153, 16–22.CrossRef

144.

Hu, Y., Duan, J., Zhan, Q., Wang, F., Lu, X., & Yang, X. D. (2012). Novel MUC1 aptamer selectively delivers cytotoxic agent to cancer cells in vitro. PLoS One, 7, e31970.PubMedCrossRef

145.

Liu, N., Zhou, C., Zhao, J., & Chen, Y. (2012). Reversal of paclitaxel resistance in epithelial ovarian carcinoma cells by a MUC1 aptamer-let-7i chimera. Cancer Investigation, 30, 577–582.PubMedCrossRef

146.

Zhao, Q., Guo, X., Nash, G. B., Stone, P. C., Hilkens, J., Rhodes, J. M., et al. (2009). Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Research, 69, 6799–6806.PubMedCrossRef

147.

Zhao, Q., Barclay, M., Hilkens, J., Guo, X., Barrow, H., Rhodes, J. M., et al. (2010). Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Molecular Cancer, 9, 154.PubMedCrossRef

Title: The role of tumour-associated MUC1 in epithelial ovarian cancer metastasis and progression
Authors: Junli Deng
Li Wang
Hongmin Chen
Lei Li
Yiming Ma
Jie Ni
Yong Li
Publication date: 01-12-2013
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 3-4/2013
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-013-9423-y

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