Mucin 1 enhances the tumor angiogenic response by activation of the AKT signaling pathway

Oncogene

Volumn 31, Issue 17, 2012, Pages 2187-2198

  Woo, J K ^a   Choi, Y ^a   Oh, S H ^b   Jeong, J H ^c   Choi, D H ^a   Seo, H S ^d   Kim, C W ^a  

^a Seoul National University   (South Korea)

^b Gachon University College of Medicine   (South Korea)

^c Korea Institute of Radiation and Medical Science   (South Korea)

^d Kyung Hee University   (South Korea)

Author keywords

angiogenesis; breast cancer; MUC1; PI3K AKT; VEGF

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; MUCIN 1; PROTEIN KINASE B; SMALL INTERFERING RNA; SOMATOMEDIN C RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SCID MOUSE; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TRANSGENIC MOUSE; TUMOR GROWTH;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, SCID; MUCIN-1; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, SOMATOMEDIN; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS; MUS MUSCULUS;

EID: 84860312605     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.410     Document Type: Article

References (54)

1. Ben-Av P, Crofford LJ, Wilder RL, Hla T. (1995). Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett 372: 83-87.
2. Borgstrom P, Hillan KJ, Sriramarao P, Ferrara N. (1996). Complete inhibition of angiogenesis and growth of microtumors by antivascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res 56: 4032-4039.
3. Brayman M, Thathiah A, Carson DD. (2004). MUC1: a multifunctional cell surface component of reproductive tissue epithelia. Reprod Biol Endocrinol 2: 4.
4. Cho JA, Yeo DJ, Son HY, Kim HW, Jung DS, Ko JK. et al. (2005). Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int J Cancer 114: 613-622.
5. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. (1996). Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 271: 736-741.
6. Duffy MJ, Shering S, Sherry F, McDermott E, O'Higgins N. (2000). CA 15-3: a prognostic marker in breast cancer. Int J Biol Markers 15: 330-333.
7. Duraisamy S, Kufe T, Ramasamy S, Kufe D. (2007). Evolution of the human MUC1 oncoprotein. Int J Oncol 31: 671-677.
8. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. (1999). Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol 237: 97-132.
9. Feldkamp MM, Lau N, Rak J, Kerbel RS, Guha A. (1999). Normoxic and hypoxic regulation of vascular endothelial growth factor (VEGF) by astrocytoma cells is mediated by Ras. Int J Cancer 81: 118-124.
10. Ferrara N. (2002). Role of vascular endothelial growth factor in physiologic and pathologic angiogenesis: therapeutic implications. Semin Oncol 29: 10-14.
11. Fessler SP, Wotkowicz MT, Mahanta SK, Bamdad C. (2009). MUC1. * is a determinant of trastuzumab (Herceptin) resistance in breast cancer cells. Breast Cancer Res Treat 118: 113-124.
12. Fontana J, Fulton D, Chen Y, Fairchild TA, McCabe TJ, Fujita N. et al. (2002). Domain mapping studies reveal that the M domain of hsp90 serves as a molecular scaffold to regulate Akt-dependent phosphorylation of endothelial nitric oxide synthase and NO release. Circ Res 90: 866-873.
13. Frank S, Hubner G, Breier G, Longaker MT, Greenhalgh DG, Werner S. (1995). Regulation of vascular endothelial growth factor expression in cultured keratinocytes. Implications for normal and impaired wound healing. J Biol Chem 270: 12607-12613.
14. Geddis AE, Fox NE, Kaushansky K. (2006). The Mpl receptor expressed on endothelial cells does not contribute significantly to the regulation of circulating thrombopoietin levels. Exp Hematol 34: 82-86.
15. Gendler SJ. (2001). MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia 6: 339-353.
16. Gendler SJ, Lancaster CA, Taylor-Papadimitriou J, Duhig T, Peat N, Burchell J. et al. (1990). Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem 265: 15286-15293.
17. Giatromanolaki A, Koukourakis MI, Sivridis E, O'Byrne K, Cox G, Thorpe PE. et al. (2000). Coexpression of MUC1 glycoprotein with multiple angiogenic factors in non-small cell lung cancer suggests coactivation of angiogenic and migration pathways. Clin Cancer Res 6: 1917-1921.
18. Guy CT, Cardiff RD, Muller WJ. (1992). Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 12: 954-961.
19. Hattrup CL, Gendler SJ. (2006). MUC1 alters oncogenic events and transcription in human breast cancer cells. Breast Cancer Res 8: R37.
20. Jemal A, Siegel R, Xu J, Ward E. (2010). Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
21. Kim B, Leventhal PS, Saltiel AR, Feldman EL. (1997). Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires mitogen-activated protein kinase activation. J Biol Chem 272: 21268-21273.
22. Kimura T, Tanaka S, Haruma K, Sumii K, Kajiyama G, Shimamoto F. et al. (2000). Clinical significance of MUC1 and E-cadherin expression, cellular proliferation, and angiogenesis at the deepest invasive portion of colorectal cancer. Int J Oncol 16: 55-64.
23. Kohno N, Hamada H, Fujioka S, Hiwada K, Yamakido M, Akiyama M. (1992). Circulating antigen KL-6 and lactate dehydrogenase for monitoring irradiated patients with lung cancer. Chest 102: 117-122.
24. Kucab JE, Dunn SE. (2003). Role of IGF-1R in mediating breast cancer invasion and metastasis. Breast Dis 17: 41-47.
25. Kurmasheva RT, Dudkin L, Billups C, Debelenko LV, Morton CL, Houghton PJ. (2009). The insulin-like growth factor-1 receptortargeting antibody, CP-751,871, suppresses tumor-derived VEGF and synergizes with rapamycin in models of childhood sarcoma. Cancer Res 69: 7662-7671.
26. Lee HY, Oh SH, Woo JK, Kim WY, Van Pelt CS, Price RE. et al. (2005). Chemopreventive effects of deguelin, a novel Akt inhibitor, on tobacco-induced lung tumorigenesis. J Natl Cancer Inst 97: 1695-1699.
27. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309.
28. Li J, Perrella MA, Tsai JC, Yet SF, Hsieh CM, Yoshizumi M. et al. (1995). Induction of vascular endothelial growth factor gene expression by interleukin-1 beta in rat aortic smooth muscle cells. J Biol Chem 270: 308-312.
29. Mikami Y, Hisatsune A, Tashiro T, Isohama Y, Katsuki H. (2009). Hypoxia enhances MUC1 expression in a lung adenocarcinoma cell line. Biochem Biophys Res Commun 379: 1060-1065.
30. Milanini-Mongiat J, Pouyssegur J, Pages G. (2002). Identification of two Sp1 phosphorylation sites for p42/p44 mitogen-activated protein kinases: their implication in vascular endothelial growth factor gene transcription. J Biol Chem 277: 20631-20639.
31. Morgillo F, Woo JK, Kim ES, Hong WK, Lee HY. (2006). Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib. Cancer Res 66: 10100-10111.
32. Okajima E, Thorgeirsson UP. (2000). Different regulation of vascular endothelial growth factor expression by the ERK and p38 kinase pathways in v-ras, v-raf, and v-myc transformed cells. Biochem Biophys Res Commun 270: 108-111.
33. Papadopoulos I, Sivridis E, Giatromanolaki A, Koukourakis MI. (2001). Tumor angiogenesis is associated with MUC1 overexpression and loss of prostate-specific antigen expression in prostate cancer. Clin Cancer Res 7: 1533-1538.
34. Parrizas M, Saltiel AR, LeRoith D. (1997). Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 30-kinase and mitogen-activated protein kinase pathways. J Biol Chem 272: 154-161.
35. Peruzzi F, Prisco M, Dews M, Salomoni P, Grassilli E, Romano G. et al. (1999). Multiple signaling pathways of the insulin-like growth factor 1 receptor in protection from apoptosis. Mol Cell Biol 19: 7203-7215.
36. Pochampalli MR, Bitler BG, Schroeder JA. (2007a). Transforming growth factor alpha dependent cancer progression is modulated by Muc1. Cancer Res 67: 6591-6598.
37. Pochampalli MR, el Bejjani RM, Schroeder JA. (2007b). MUC1 is a novel regulator of ErbB1 receptor trafficking. Oncogene 26: 1693-1701.
38. Pollak MN. (2004). Insulin-like growth factors and neoplasia. Novartis Found Symp 262: 84-98; discussion 98-107, 265-108.
39. Pore N, Liu S, Shu HK, Li B, Haas-Kogan D, Stokoe D. et al. (2004 Sp1 is involved in Akt-mediated induction of VEGF expression through an HIF-1-independent mechanism. Mol Biol Cell 15: 4841-4853.
40. Poulaki V, Mitsiades CS, McMullan C, Sykoutri D, Fanourakis G, Kotoula V. et al. (2003). Regulation of vascular endothelial growth factor expression by insulin-like growth factor I in thyroid carcinomas. J Clin Endocrinol Metab 88: 5392-5398.
41. Raina D, Kharbanda S, Kufe D. (2004). The MUC1 oncoprotein activates the anti-apoptotic phosphoinositide 3-kinase/Akt and BclxL pathways in rat 3Y1 fibroblasts. J Biol Chem 279: 20607-20612.
42. Ren J, Raina D, Chen W, Li G, Huang L, Kufe D. (2006). MUC1 oncoprotein functions in activation of fibroblast growth factor receptor signaling. Mol Cancer Res 4: 873-883.
43. Risau W. (1997). Mechanisms of angiogenesis. Nature 386: 671-674.
44. Sachdeva M, Mo YY. (2010). MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res 70: 378-387.
45. Sakamoto H, Yonezawa S, Utsunomiya T, Tanaka S, Kim YS, Sato E. (1997). Mucin antigen expression in gastric carcinomas of young and old adults. Hum Pathol 28: 1056-1065.
46. Sorokin LM, Pausch F, Frieser M, Kroger S, Ohage E, Deutzmann R. (1997). Developmental regulation of the laminin alpha5 chain suggests a role in epithelial and endothelial cell maturation. Dev Biol 189: 285-300.
47. Tang Y, Zhang D, Fallavollita L, Brodt P. (2003). Vascular endothelial growth factor C expression and lymph node metastasis are regulated by the type I insulin-like growth factor receptor. Cancer Res 63: 1166-1171.
48. Wang BF, Cheng YA, Dang SS. (2009). [Angiogenesis inhibitory effect of saikosaponin-d on chicken embryo]. Zhongguo Zhong Xi Yi Jie He Za Zhi 29: 425-429.
49. Wei X, Xu H, Kufe D. (2006). MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell 21: 295-305.
50. Werner H, Le Roith D. (2000). New concepts in regulation and function of the insulin-like growth factors: implications for understanding normal growth and neoplasia. Cell Mol Life Sci 57: 932-942.
51. Yin L, Kharbanda S, Kufe D. (2007). Mucin 1 oncoprotein blocks hypoxia-inducible factor 1alpha activation in a survival response to hypoxia. J Biol Chem 282: 257-266.
52. Yoshiji H, Harris SR, Thorgeirsson UP. (1997). Vascular endothelial growth factor is essential for initial but not continued in vivo growth of human breast carcinoma cells. Cancer Res 57: 3924-3928.
53. Yu H, Wu J, Li H, Wang Z, Chen X, Tian Y. et al. (2007). Inhibition of corneal neovascularization by recombinant adenovirus-mediated sFlk-1 expression. Biochem Biophys Res Commun 361: 946-952.
54. Yuen JS, Cockman ME, Sullivan M, Protheroe A, Turner GD, oberts IS. et al. (2007). The VHL tumor suppressor inhibits expression of the IGF1R and its loss induces IGF1R upregulation in human clear cell renal carcinoma. Oncogene 26: 6499-6508