Impact of MUC1 mucin downregulation in the phenotypic characteristics of MKN45 gastric carcinoma cell line

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Costa, Natália R ^a   Paulo, Paula ^a   Caffrey, Thomas ^b   Hollingsworth, Michael A ^b   Santos Silva, Filipe ^a,c  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c University of Porto   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN B; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 5; CELL ADHESION MOLECULE; CLUSTERIN; DECAY ACCELERATING FACTOR; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE DELTA 4; EPSILON SARCOGLYCAN; GALECTIN 1; GALECTIN 4; GUANOSINE DIPHOSPHATE MANNOSE; GUANOSINE DIPHOSPHATE MANNOSE 4,6 DEHYDRATASE; HAPTOCORRIN; KALLIKREIN 6; LIPOCORTIN 4; MUCIN 1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SHORT HAIRPIN RNA; TETRASPANIN; TETRASPANIN 8; TETRAZOLIUM; TRANSCRIPTION FACTOR SP2; TRANSFORMING GROWTH FACTOR BETA1; TRYPSIN; TRYPSIN 2; UBIQUITIN CONJUGATING ENZYME; UNCLASSIFIED DRUG; VILLIN; VILLIN 1; MUC1 PROTEIN, HUMAN; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL AGGREGATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; MICROARRAY ANALYSIS; MOUSE; NICK END LABELING; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; RNA INTERFERENCE; STOMACH CARCINOMA; TUMOR GROWTH; VARIABLE NUMBER OF TANDEM REPEAT; WESTERN BLOTTING; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STOMACH TUMOR; TUMOR CELL LINE;

MUS;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA PRIMERS; DOWN-REGULATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IN SITU NICK-END LABELING; MICE; MICE, NUDE; MUCIN-1; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; STOMACH NEOPLASMS;

EID: 80355136460     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026970     Document Type: Article

References (62)

1. Power DG, Kelsen DP, Shah MA, (2010) Advanced gastric cancer--slow but steady progress. Cancer Treat Rev 36: 384-392.
2. Patton S, Gendler SJ, Spicer AP, (1995) The epithelial mucin, MUC1, of milk, mammary gland and other tissues. Biochim Biophys Acta 1241: 407-423.
3. Yonezawa S, Sato E, (1997) Expression of mucin antigens in human cancers and its relationship with malignancy potential. Pathol Int 47: 813-830.
4. Klinge CM, Radde BN, Imbert-Fernandez Y, Teng Y, Ivanova MM, et al. (2011) Targeting the intracellular MUC1 C-terminal domain inhibits proliferation and estrogen receptor transcriptional activity in lung adenocarcinoma cells. Mol Cancer Ther.
5. Ye Q, Yan Z, Liao X, Li Y, Yang J, et al. (2011) MUC1 induces metastasis in esophageal squamous cell carcinoma by upregulating matrix metalloproteinase 13. Lab Invest 91: 778-787.
6. Bafna S, Kaur S, Batra SK, (2010) Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29: 2893-2904.
7. Resende C, Thiel A, Machado JC, Ristimaki A, (2011) Gastric cancer: basic aspects. Helicobacter 16 (Suppl 1): 38-44.
8. Park JH, Nishidate T, Kijima K, Ohashi T, Takegawa K, et al. (2010) Critical roles of mucin 1 glycosylation by transactivated polypeptide N-acetylgalactosaminyltransferase 6 in mammary carcinogenesis. Cancer Res 70: 2759-2769.
9. Xu Y, Zhang L, Hu G, (2009) Potential application of alternatively glycosylated serum MUC1 and MUC5AC in gastric cancer diagnosis. Biologicals 37: 18-25.
10. Inagaki Y, Tang W, Xu H, Nakata M, Mafune K, et al. (2011) Sustained aberrant localization of KL-6 mucin and beta-catenin at the invasion front of human gastric cancer cells. Anticancer Res 31: 535-542.
11. Benjamin JB, Jayanthi V, Devaraj H, (2010) MUC1 expression and its association with other aetiological factors and localization to mitochondria in preneoplastic and neoplastic gastric tissues. Clin Chim Acta 411: 2067-2072.
12. Kohlgraf KG, Gawron AJ, Higashi M, Meza JL, Burdick MD, et al. (2003) Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line. Cancer Res 63: 5011-5020.
13. Hattrup CL BJ, Kotlarczyk KL, Madsen CS, Hentz JG, et al. (2008) The MUC1 Cytoplasmic Tail and Tandem Repeat Domains Contribute to Mammary Oncogenesis in FVB Mice. Breast Cancer 1: 57-63.
14. Gendler S, Taylor-Papadimitriou J, Duhig T, Rothbard J, Burchell J, (1988) A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 263: 12820-12823.
15. Hayashi T, Takahashi T, Motoya S, Ishida T, Itoh F, et al. (2001) MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion 63 (Suppl 1): 87-92.
16. Yu LG, Andrews N, Zhao Q, McKean D, Williams JF, et al. (2007) Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 282: 773-781.
17. Shen Q, Rahn JJ, Zhang J, Gunasekera N, Sun X, et al. (2008) MUC1 initiates Src-CrkL-Rac1/Cdc42-mediated actin cytoskeletal protrusive motility after ligating intercellular adhesion molecule-1. Mol Cancer Res 6: 555-567.
18. Rahn JJ, Chow JW, Horne GJ, Mah BK, Emerman JT, et al. (2005) MUC1 mediates transendothelial migration in vitro by ligating endothelial cell ICAM-1. Clin Exp Metastasis 22: 475-483.
19. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, et al. (2009) Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69: 6799-6806.
20. Zhao Q, Barclay M, Hilkens J, Guo X, Barrow H, et al. (2010) Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Mol Cancer 9: 154.
21. Singh PK, Hollingsworth MA, (2006) Cell surface-associated mucins in signal transduction. Trends Cell Biol 16: 467-476.
22. Carraway KL, 3rd, Funes M, Workman HC, Sweeney C, (2007) Contribution of membrane mucins to tumor progression through modulation of cellular growth signaling pathways. Curr Top Dev Biol 78: 1-22.
23. Li Y, Chen W, Ren J, Yu WH, Li Q, et al. (2003) DF3/MUC1 signaling in multiple myeloma cells is regulated by interleukin-7. Cancer Biol Ther 2: 187-193.
24. Li Q, Ren J, Kufe D, (2004) Interaction of human MUC1 and beta-catenin is regulated by Lck and ZAP-70 in activated Jurkat T cells. Biochem Biophys Res Commun 315: 471-476.
25. Wei X, Xu H, Kufe D, (2006) MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell 21: 295-305.
26. Ahmad R, Raina D, Joshi MD, Kawano T, Ren J, et al. (2009) MUC1-C oncoprotein functions as a direct activator of the nuclear factor-kappaB p65 transcription factor. Cancer Res 69: 7013-7021.
27. Raina D, Ahmad R, Kumar S, Ren J, Yoshida K, et al. (2006) MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J 25: 3774-3783.
28. Huang L, Liao X, Beckett M, Li Y, Khanna KK, et al. (2010) MUC1-C Oncoprotein Interacts Directly with ATM and Promotes the DNA Damage Response to Ionizing Radiation. Genes Cancer 1: 239-250.
29. Guang W, Kim KC, Lillehoj EP, (2009) MUC1 mucin interacts with calcium-modulating cyclophilin ligand. Int J Biochem Cell Biol 41: 1354-1360.
30. Taylor-Papadimitriou J, Burchell J, Miles DW, Dalziel M, (1999) MUC1 and cancer. Biochim Biophys Acta 1455: 301-313.
31. Motoyama T, Hojo H, Watanabe H, (1986) Comparison of seven cell lines derived from human gastric carcinomas. Acta Pathol Jpn 36: 65-83.
32. Kinsella TM, Nolan GP, (1996) Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 7: 1405-1413.
33. Tuschl T, (2001) RNA interference and small interfering RNAs. Chembiochem 2: 239-245.
34. Ginzinger DG, (2002) Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol 30: 503-512.
35. Tsutsumida H, Swanson BJ, Singh PK, Caffrey TC, Kitajima S, et al. (2006) RNA interference suppression of MUC1 reduces the growth rate and metastatic phenotype of human pancreatic cancer cells. Clin Cancer Res 12: 2976-2987.
36. Singh PK, Wen Y, Swanson BJ, Shanmugam K, Kazlauskas A, et al. (2007) Platelet-derived growth factor receptor beta-mediated phosphorylation of MUC1 enhances invasiveness in pancreatic adenocarcinoma cells. Cancer Res 67: 5201-5210.
37. Behrens ME, Grandgenett PM, Bailey JM, Singh PK, Yi CH, et al. (2010) The reactive tumor microenvironment: MUC1 signaling directly reprograms transcription of CTGF. Oncogene 29: 5667-5677.
38. Hattrup CL, Gendler SJ, (2006) MUC1 alters oncogenic events and transcription in human breast cancer cells. Breast Cancer Res 8: R37.
39. Yuan Z, Liu X, Wong S, Machan JT, Chung MA, (2009) MUC1 Knockdown With RNA Interference Inhibits Pancreatic Cancer Growth. J Surg Res 157: e39-46.
40. Lillehoj EP, Lu W, Kiser T, Goldblum SE, Kim KC, (2007) MUC1 inhibits cell proliferation by a beta-catenin-dependent mechanism. Biochim Biophys Acta 1773: 1028-1038.
41. Li X, Wang L, Nunes DP, Troxler RF, Offner GD, (2005) Suppression of MUC1 synthesis downregulates expression of the epidermal growth factor receptor. Cancer Biol Ther 4: 968-973.
42. Nathalie HV, Chris P, Serge G, Catherine C, Benjamin B, et al. (2009) High kallikrein-related peptidase 6 in non-small cell lung cancer cells: an indicator of tumour proliferation and poor prognosis. J Cell Mol Med 13: 4014-4022.
43. Satelli A, Rao PS, Thirumala S, Rao US, (2010) Galectin-4 functions as a tumor suppressor of human colorectal cancer. Int J Cancer.
44. Satelli A, Rao PS, Thirumala S, Rao US, (2011) Galectin-4 functions as a tumor suppressor of human colorectal cancer. Int J Cancer 129: 799-809.
45. Chaturvedi R, Srivastava RK, Hisatsune A, Shankar S, Lillehoj EP, et al. (2005) Augmentation of Fas ligand-induced apoptosis by MUC1 mucin. Int J Oncol 26: 1169-1176.
46. Kawano T, Ahmad R, Nogi H, Agata N, Anderson K, et al. (2008) MUC1 oncoprotein promotes growth and survival of human multiple myeloma cells. Int J Oncol 33: 153-159.
47. Agata N, Ahmad R, Kawano T, Raina D, Kharbanda S, et al. (2008) MUC1 oncoprotein blocks death receptor-mediated apoptosis by inhibiting recruitment of caspase-8. Cancer Res 68: 6136-6144.
48. Ren J, Agata N, Chen D, Li Y, Yu WH, et al. (2004) Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 5: 163-175.
49. Wang Q, Li M, Wang Y, Zhang Y, Jin S, et al. (2008) RNA interference targeting CML66, a novel tumor antigen, inhibits proliferation, invasion and metastasis of HeLa cells. Cancer Lett 269: 127-138.
50. Aubert S, Fauquette V, Hemon B, Lepoivre R, Briez N, et al. (2009) MUC1, a new hypoxia inducible factor target gene, is an actor in clear renal cell carcinoma tumor progression. Cancer Res 69: 5707-5715.
51. Yuan Z, Wong S, Borrelli A, Chung MA, (2007) Down-regulation of MUC1 in cancer cells inhibits cell migration by promoting E-cadherin/catenin complex formation. Biochem Biophys Res Commun 362: 740-746.
52. Schroeder JA, Adriance MC, Thompson MC, Camenisch TD, Gendler SJ, (2003) MUC1 alters beta-catenin-dependent tumor formation and promotes cellular invasion. Oncogene 22: 1324-1332.
53. Gao J, McConnell MJ, Yu B, Li J, Balko JM, et al. (2009) MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol 35: 337-345.
54. McDermott KM, Crocker PR, Harris A, Burdick MD, Hinoda Y, et al. (2001) Overexpression of MUC1 reconfigures the binding properties of tumor cells. Int J Cancer 94: 783-791.
55. Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, et al. (1996) The breast mucin MUCI as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res 56: 4244-4249.
56. Nath D, Hartnell A, Happerfield L, Miles DW, Burchell J, et al. (1999) Macrophage-tumour cell interactions: identification of MUC1 on breast cancer cells as a potential counter-receptor for the macrophage-restricted receptor, sialoadhesin. Immunology 98: 213-219.
57. Wesseling J, van der Valk SW, Vos HL, Sonnenberg A, Hilkens J, (1995) Episialin (MUC1) overexpression inhibits integrin-mediated cell adhesion to extracellular matrix components. J Cell Biol 129: 255-265.
58. Wesseling J, van der Valk SW, Hilkens J, (1996) A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol Biol Cell 7: 565-577.
59. Klucky B, Mueller R, Vogt I, Teurich S, Hartenstein B, et al. (2007) Kallikrein 6 induces E-cadherin shedding and promotes cell proliferation, migration, and invasion. Cancer Res 67: 8198-8206.
60. Singh PK, Behrens ME, Eggers JP, Cerny RL, Bailey JM, et al. (2008) Phosphorylation of MUC1 by Met modulates interaction with p53 and MMP1 expression. J Biol Chem 283: 26985-26995.
61. Henkhaus RS GE, Ignatenko NA, (2008) Kallikrein 6 is a mediator of K-RAS-dependent migration of colon carcinoma cells. Biological Chemistry 389 (6): 757-764.
62. Ling Y, Maile LA, Lieskovska J, Badley-Clarke J, Clemmons DR, (2005) Role of SHPS-1 in the regulation of insulin-like growth factor I-stimulated Shc and mitogen-activated protein kinase activation in vascular smooth muscle cells. Mol Biol Cell 16: 3353-3364.