MUC1 enhances hypoxia-driven angiogenesis through the regulation of multiple proangiogenic factors

Oncogene

Volumn 32, Issue 39, 2013, Pages 4614-4621

  Kitamoto, S ^a   Yokoyama, S ^a   Higashi, M ^a   Yamada, N ^a   Takao, S ^b   Yonezawa, S ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

angiogenesis; hypoxia; MUC1; mucin; pancreatic cancer

Indexed keywords

ANGIOGENIC FACTOR; BETA CATENIN; CONNECTIVE TISSUE GROWTH FACTOR; MUCIN 1; NEUTRALIZING ANTIBODY; PLATELET DERIVED GROWTH FACTOR B; PROTEIN P53; SMALL INTERFERING RNA; VASCULOTROPIN A;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CELL; CELL HYPOXIA; CELL INTERACTION; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOPLASM; ENDOTHELIUM CELL; GENE FUNCTION; GENE INDUCTION; GENE LOCATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; METASTASIS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TUMOR MICROENVIRONMENT;

ANGIOGENIC PROTEINS; CARCINOMA; CELL DIVISION; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CELL NUCLEUS; CONNECTIVE TISSUE GROWTH FACTOR; CULTURE MEDIA, CONDITIONED; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MUCIN-1; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; OXIDATIVE STRESS; PANCREATIC NEOPLASMS; PEPTIDE FRAGMENTS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-SIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84884902758     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.478     Document Type: Article

References (40)

1. Hidalgo M. Pancreatic cancer. N Engl J Med 2010; 362: 16051617.
2. Harris AL. Hypoxiaa key regulatory factor in tumour growth. Nat Rev Cancer 2002; 2: 3847.
3. Semenza GL. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med 2003; 54: 1728.
4. Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 2004; 4: 437447.
5. Chang Q, Jurisica I, Do T, Hedley DW. Hypoxia predicts aggressive growth and spontaneous metastasis formation from orthotopically grown primary xenografts of human pancreatic cancer. Cancer Res 2011; 71: 31103120.
6. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 2010; 16: 59285935.
7. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 2007; 26: 225239.
8. Dewhirst MW, Cao Y, Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat Rev Cancer 2008; 8: 425437.
9. Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2012; 12: 922.
10. Macao B, Johansson DG, Hansson GC, Hard T. Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 2006; 13: 7176.
11. Levitin F, Stern O, Weiss M, Gil-Henn C, Ziv R, Prokocimer Z et al. The MUC1 SEA module is a self-cleaving domain. J Biol Chem 2005; 280: 3337433386.
12. Bhaskar KR, Garik P, Turner BS, Bradley JD, Bansil R, Stanley HE et al. Viscous fingering of HCl through gastric mucin. Nature 1992; 360: 458461.
13. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal Immunol 2008; 1: 183197.
14. Yonezawa S, Higashi M, Yamada N, Yokoyama S, Kitamoto S, Kitajima S et al. Mucins in human neoplasms: clinical pathology, gene expression and diagnostic application. Pathol Int 2011; 61: 697716.
15. Hollingsworth MA, Swanson BJ. Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 2004; 4: 4560.
16. Kufe DW. Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 2009; 9: 874885.
17. Carson DD. The cytoplasmic tail of MUC1: a very busy place. Sci Signal 2008; 1: pe35.
18. Aubert S, Fauquette V, Hemon B, Lepoivre R, Briez N, Bernard D et al. MUC1, a new hypoxia inducible factor target gene, is an actor in clear renal cell carcinoma tumor progression. Cancer Res 2009; 69: 57075715.
19. Mikami Y, Hisatsune A, Tashiro T, Isohama Y, Katsuki H. Hypoxia enhances MUC1 expression in a lung adenocarcinoma cell line. Biochem Biophys Res Commun 2009; 379: 10601065.
20. Kaira K, Nakagawa K, Ohde Y, Okumura T, Takahashi T, Murakami H et al. Depolarized MUC1 expression is closely associated with hypoxic markers and poor outcome in resected non-small cell lung cancer. Int J Surg Pathol 2011; 20: 223232.
21. Zanetti JS, Soave DF, Oliveira-Costa JP, da Silveira GG, Ramalho LN, Garcia SB et al. The role of tumor hypoxia in MUC1-positive breast carcinomas. Virchows Arch 2011; 459: 367375.
22. Kaira K, Okumura T, Nakagawa K, Ohde Y, Takahashi T, Murakami H et al. MUC1 Expression in pulmonary metastatic tumors: a comparison of primary lung cancer. Pathol Oncol Res 2012; 18: 439447.
23. Giatromanolaki A, Koukourakis MI, Sivridis E, OByrne K, Cox G, Thorpe PE et al. Coexpression of MUC1 glycoprotein with multiple angiogenic factors in non-small cell lung cancer suggests coactivation of angiogenic and migration pathways. Clin Cancer Res 2000; 6: 19171921.
24. Papadopoulos I, Sivridis E, Giatromanolaki A, Koukourakis MI. Tumor angiogenesis is associated with MUC1 overexpression and loss of prostatespecific antigen expression in prostate cancer. Clin Cancer Res 2001; 7: 15331538.
25. Behrens ME, Grandgenett PM, Bailey JM, Singh PK, Yi CH, Yu F et al. The reactive tumor microenvironment: MUC1 signaling directly reprograms transcription of CTGF. Oncogene 2010; 29: 56675677.
26. Bennewith KL, Huang X, Ham CM, Graves EE, Erler JT, Kambham N et al. The role of tumor cell-derived connective tissue growth factor (CTGF/CCN2) in pancreatic tumor growth. Cancer Res 2009; 69: 775784.
27. Shimo T, Kubota S, Kondo S, Nakanishi T, Sasaki A, Mese H et al. Connective tissue growth factor as a major angiogenic agent that is induced by hypoxia in a human breast cancer cell line. Cancer Lett 2001; 174: 5764.
28. Sahraei M, Roy LD, Curry JM, Teresa TL, Nath S, Besmer D et al. MUC1 regulates PDGFA expression during pancreatic cancer progression. Oncogene 2012; 31: 49354945.
29. Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL et al. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 2011; 30: 14491459.
30. Yao M, Zhang W, Zhang Q, Xing L, Xu A, Liu Q et al. Overexpression of MUC1 enhances proangiogenic activity of non-small-cell lung cancer cells through activation of Akt and extracellular signal-regulated kinase pathways. Lung 2011; 189: 453460.
31. Woo JK, Choi Y, Oh SH, Jeong JH, Choi DH, Seo HS et al. Mucin 1 enhances the tumor angiogenic response by activation of the AKT signaling pathway. Oncogene 2011; 31: 21872198.
32. Yin L, Kharbanda S, Kufe D. Mucin 1 oncoprotein blocks hypoxia-inducible factor 1alpha activation in a survival response to hypoxia. J Biol Chem 2007; 282: 257266.
33. Chu CY, Chang CC, Prakash E, Kuo ML. Connective tissue growth factor (CTGF) and cancer progression. J Biomed Sci 2008; 15: 675685.
34. Dornhofer N, Spong S, Bennewith K, Salim A, Klaus S, Kambham N et al. Connective tissue growth factor-specific monoclonal antibody therapy inhibits pancreatic tumor growth and metastasis. Cancer Res 2006; 66: 58165827.
35. Higgins DF, Biju MP, Akai Y, Wutz A, Johnson RS, Haase VH. Hypoxic induction of Ctgf is directly mediated by Hif-1. Am J Physiol Renal Physiol 2004; 287: F1223F1232.
36. Sakamoto H, Yonezawa S, Utsunomiya T, Tanaka S, Kim YS, Sato E. Mucin antigen expression in gastric carcinomas of young and old adults. Hum Pathol 1997; 28: 10561065.
37. Furukawa T, Duguid WP, Rosenberg L, Viallet J, Galloway DA, Tsao MS. Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am J Pathol 1996; 148: 17631770.
38. Ouyang H, Mou L, Luk C, Liu N, Karaskova J, Squire J et al. Immortal human pancreatic duct epithelial cell lines with near normal genotype and phenotype. Am J Pathol 2000; 157: 16231631.
39. Yonezawa S, Kitajima S, Higashi M, Osako M, Horinouchi M, Yokoyama S et al. A novel anti-MUC1 antibody against the MUC1 cytoplasmic tail domain: use in sensitive identification of poorly differentiated cells in adenocarcinoma of the stomach. Gastric Cancer (e-pub ahead of print 12 January 2012; doi:10.1007/S10120-011-0125-2).
40. Kitamoto S, Yokoyama S, Higashi M, Yamada N, Matsubara S, Takao S et al. Expression of MUC17 is regulated by HIF1alpha-mediated hypoxic responses and requires a methylation-free hypoxia responsible element in pancreatic cancer. PloS one 2012; 7: e44108.