An aberrant nuclear localization of E-cadherin is a potent inhibitor of Wnt/ß-catenin-elicited promotion of the cancer stem cell phenotype

Oncogenesis

Volumn 4, Issue 6, 2015, Pages

  Su, Y J ^a   Chang, Y W ^a,b   Lin, W H ^a,b   Liang, C L ^a   Lee, J L ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETA CATENIN; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; PROTEIN; SHORT HAIRPIN RNA; TCF4 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER STEM CELL; CARCINOGENICITY; CELL CLONE; CELL FRACTIONATION; CELL PROLIFERATION ASSAY; CELL STIMULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECTOPIC EXPRESSION; ENDOCYTOSIS; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; LUNG CANCER; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SUPERNATANT; TISSUE MICROARRAY; TRANSCRIPTION INITIATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

EID: 84989338265     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2015.17     Document Type: Article

References (54)

1. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: Mirage or reality? Nat Med 2009; 15: 1010-1012.
2. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
3. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
4. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
5. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67: 1030-1037.
6. Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006; 25: 1696-1708.
7. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828.
8. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445: 111-115.
9. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumorinitiating features. Proc Natl Acad Sci USA 2009; 106: 13820-13825.
10. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
11. Blanpain C, Horsley V, Fuchs E.. Epithelial stem cells: Turning over new leaves. Cell 2007; 128: 445-458.
12. van der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009; 71: 241-260.
13. Alison MR, Islam S. Attributes of adult stem cells. J Pathol 2009; 217: 144-160.
14. Polakis P. Wnt signaling and cancer. Genes Dev 2000; 14: 1837-1851.
15. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850.
16. Stewart DJ. Wnt signaling pathway in non-small cell lung cancer. J Natl Cancer Inst 2014; 106: Djt356.
17. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, Borovski T et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010; 12: 468-476.
18. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008; 452: 650-653.
19. Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010; 6: 568-577.
20. Bisson I, Prowse DM. WNT signaling regulates self-renewal and differentiation of prostate cancer cells with stem cell characteristics. Cell Res 2009; 19: 683-697.
21. Junghans D, Haas IG, Kemler R. Mammalian cadherins and protocadherins: About cell death, synapses and processing. Curr Opin Cell Biol 2005; 17: 446-452.
22. Cowin P, Rowlands TM, Hatsell SJ. Cadherins and catenins in breast cancer. Curr Opin Cell Biol 2005; 17: 499-508.
23. Li J, Zhou BP. Activation of ß-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011; 11: 49.
24. Becker KF, Atkinson MJ, Reich U, Huang HH, Nekarda H, Siewert JR et al. Exon skipping in the E-cadherin gene transcript in metastatic human gastric carcinomas. Hum Mol Genet 1993; 2: 803-804.
25. Strathdee G. Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin Cancer Biol 2002; 12: 373-379.
26. Jiang W, Hiscox S. beta-catenin-cell adhesion and beyond (review). Int J Oncol 1997; 11: 635-641.
27. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat Cell Biol 2002; 4: 222-231.
28. Shen Y, Hirsch DS, Sasiela CA, Wu WJ. Cdc42 regulates E-cadherin ubiquitination and degradation through an epidermal growth factor receptor to Src-mediated pathway. J Biol Chem 2008; 283: 5127-5137.
29. Richards FM, McKee SA, Rajpar MH, Cole TR, Evans DG, Jankowski JA et al. Germline E-cadherin gene (CDH1) mutations predispose to familial gastric cancer and colorectal cancer. Hum Mol Genet 1999; 8: 607-610.
30. Efstathiou JA, Liu D, Wheeler JM, Kim HC, Beck NE, Ilyas M et al. Mutated epithelial cadherin is associated with increased tumorigenicity and loss of adhesion and of responsiveness to the motogenic trefoil factor 2 in colon carcinoma cells. Proc Natl Acad Sci USA 1999; 96: 2316-2321.
31. Han AC, Soler AP, Tang CK, Knudsen KA, Salazar H. Nuclear localization of E-cadherin expression in Merkel cell carcinoma. Arch Pathol Lab Med 2000; 124: 1147-1151.
32. Moon KC, Cho SY, Lee HS, Jeon YK, Chung JH, Jung KC et al. Distinct expression patterns of E-cadherin and beta-catenin in signet ring cell carcinoma components of primary pulmonary adenocarcinoma. Arch Pathol Lab Med 2006; 130: 1320-1325.
33. Serra S, Salahshor S, Fagih M, Niakosari F, Radhi JM, Chetty R. Nuclear expression of E-cadherin in solid pseudopapillary tumors of the pancreas. JOP 2007; 8: 296-303.
34. Camp RL, Rimm EB, Rimm DL. Met expression is associated with poor outcome in patients with axillary lymph node negative breast carcinoma. Cancer 1999; 86: 2259-2265.
35. Lee JL, Chang CJ, Wu SY, Sargan DR, Lin CT. Secreted frizzled-related protein 2 (SFRP2) is highly expressed in canine mammary gland tumors but not in normal mammary glands. Breast Cancer Res Treat 2004; 84: 139-149.
36. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y et al. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002; 108: 837-847.
37. Graham TA, Weaver C, Mao F, Kimelman D, Xu W. Crystal structure of a betacatenin/ Tcf complex. Cell 2000; 103: 885-896.
38. Daniels DL, Weis WI. ICAT inhibits beta-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol Cell 2002; 10: 573-584.
39. Schuijers J, Mokry M, Hatzis P, Cuppen E, Clevers H. Wnt-induced transcriptional activation is exclusively mediated by TCF/LEF. EMBO J 2014; 33: 146-156.
40. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J Biol Chem 1999; 274: 36734-36740.
41. Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004; 303: 1483-1487.
42. Coluccia AM, Benati D, Dekhil H, De Filippo A, Lan C, Gambacorti-Passerini C. SKI-606 decreases growth and motility of colorectal cancer cells by preventing pp60(c-Src)-dependent tyrosine phosphorylation of beta-catenin and its nuclear signaling. Cancer Res 2006; 66: 2279-2286.
43. Yokoyama N, Malbon CC. Dishevelled-2 docks and activates Src in a Wntdependent manner. J Cell Sci 2009; 122: 4439-4451.
44. Chen Q, Su Y, Wesslowski J, Hagemann AI, Ramialison M, Wittbrodt J et al. Tyrosine phosphorylation of LRP6 by Src and Fer inhibits Wnt/beta-catenin signalling. EMBO Rep 2014; 15: 1254-1267.
45. Wu D, Pan W. GSK3: A multifaceted kinase in Wnt signaling. Trends Biochem Sci 2010; 35: 161-168.
46. Chen XF, Zhang HT, Qi QY, Sun MM, Tao LY. Expression of E-cadherin and nm23 is associated with the clinicopathological factors of human non-small cell lung cancer in China. Lung Cancer 2005; 48: 69-76.
47. Liu L, Zhu XD, Wang WQ, Shen Y, Qin Y, Ren ZG et al. Activation of beta-catenin by hypoxia in hepatocellular carcinoma contributes to enhanced metastatic potential and poor prognosis. Clin Cancer Res 2010; 16: 2740-2750.
48. Kuphal S, Poser I, Jobin C, Hellerbrand C, Bosserhoff AK. Loss of E-cadherin leads to upregulation of NFkappaB activity in malignant melanoma. Oncogene 2004; 23: 8509-8519.
49. Herzig M, Savarese F, Novatchkova M, Semb H, Christofori G. Tumor progression induced by the loss of E-cadherin independent of beta-catenin/Tcf-mediated Wnt signaling. Oncogene 2007; 26: 2290-2298.
50. den Elzen N, Buttery CV, Maddugoda MP, Ren G, Yap AS. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol Biol Cell 2009; 20: 3740-3750.
51. Lee JL, Lin CT, Chueh LL, Chang CJ. Autocrine/paracrine secreted Frizzled-related protein 2 induces cellular resistance to apoptosis: A possible mechanism of mammary tumorigenesis. J Biol Chem 2004; 279: 14602-14609.
52. Su YJ, Lai HM, Chang YW, Chen GY, Lee JL. Direct reprogramming of stem cell properties in colon cancer cells by CD44. EMBO J 2011; 30: 3186-3199.
53. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
54. Lee JL, Wang MJ, Chen JY. Acetylation and activation of STAT3 mediated by nuclear translocation of CD44. J Cell Biol 2009; 185: 949-957.