The zinc transporter LIV-1 is a novel regulator of stemness in pancreatic cancer cells

Scandinavian Journal of Gastroenterology

Volumn 49, Issue 2, 2014, Pages 215-221

  Unno, Jun ^a   Masamune, Atsushi ^a   Hamada, Shin ^a   Shimosegawa, Tooru ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer stem cells; Niche; SiRNA; Transporter; Zinc

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; LIN28; MICRORNA; MICRORNA 149; MICRORNA 424; MICRORNA 7; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UVOMORULIN; ZINC TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INCIDENCE; CANCER STEM CELL; CARCINOGENESIS; CELL MIGRATION; CELL MIGRATION ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LIV 1 GENE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS CANCER; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR SPHEROID; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CADHERINS; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICRORNAS; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SPHEROIDS, CELLULAR; UP-REGULATION;

EID: 84892692044     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.3109/00365521.2013.865075     Document Type: Article

References (38)

1. Brand RE, Tempero MA. Pancreatic cancer. Curr Opin Oncol 1998;10:362-6.
2. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30.
3. Hidalgo M. Pancreatic cancer. N Engl J Med 2010;362: 1605-17.
4. Brittan M, Wright NA. Gastrointestinal stem cells. J Pathol 2002;197:492-509.
5. MageeJA,PiskounovaE,MorrisonSJ. Cancerstemcells:impact, heterogeneity, and uncertainty Cancer Cell 2012;21:283-96.
6. Cho RW, Clarke MF. Recent advances in cancer stem cells. Curr Opin Genet Dev 2008;18:48-53.
7. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007;67:1030-7.
8. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007;1:313-23.
9. Hamada S, Masamune A, Takikawa T, Suzuki N, Kikuta K, Hirota M, et al. Pancreatic stellate cells enhance stem cell-like phenotypes in pancreatic cancer cells. Biochem Biophys Res Commun 2012;421:349-54.
10. Taylor KM, Hiscox S, Nicholson RI. Zinc transporter LIV-1: a link between cellular development and cancer progression. Trends Endocrinol Metab 2004;15:461-3.
11. Manning DL, Daly RJ, Lord PG, Kelly KF, Green CD. Effects of oestrogen on the expression of a 4. 4 kb mRNA in the ZR-75-1 human breast cancer cell line. Mol Cell Endocrinol 1988;59:205-12.
12. Manning DL, Robertson JF, Ellis IO, Elston CW, McClelland RA, Gee JM, et al. Oestrogen-regulated genes in breast cancer: association of pLIV1 with lymph node involvement. Eur J Cancer 1994;30A:675-8.
13. Grattan BJ, Freake HC. Zinc and cancer: implications for LIV-1 in breast cancer. Nutrients 2012;4:648-75.
14. Kasper G, Weiser AA, Rump A, Sparbier K, Dahl E, Hartmann A, et al. Expression levels of the putative zinc transporter LIV-1 are associated with a better outcome of breast cancer patients. Int J Cancer 2005;117:961-73.
15. Lue HW, Yang X, Wang R, Qian W, Xu RZ, Lyles R, et al. LIV-1 promotes prostate cancer epithelial-to-mesenchymal transition and metastasis through HB-EGF shedding and EGFR-mediated ERK signaling. PLoS One 2011;6:e27720.
16. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, Chu G, et al. Epithelial to mesenchymal transition (EMT) in human prostate cancer: lessons learned from ARCaP model. Clin Exp Metastasis 2008;25:601-10.
17. Zhao L, Chen W, Taylor KM, Cai B, Li X. LIV-1-suppression inhibits HeLa cell invasion by targeting ERK1/2-Snail/Slug pathway. Biochem Biophys Res Commun 2007;363:82-8.
18. Unno J, Satoh K, Hirota M, Kanno A, Hamada S, Ito H, et al. LIV-1 enhances the aggressive phenotype through the induction of epithelial to mesenchymal transition in human pancreatic carcinoma cells. Int J Oncol 2009;35:813-21.
19. Shen R, Xie F, Shen H, liu Q, Zheng T, Kou X, et al. Negative correlation of LIV-1 and E-cadherin expression in hepatocellular carcinoma cells. PLoS One 2013;8:e56542.
20. Yamashita S, Miyagi C, Fukada T, Kagara N, Che YS, Hirano T. Zinc transporter LIVI controls epithelialmesenchymal transition in zebrafish gastrula organizer. Nature 2004;429:298-302.
21. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The Epithelial-mesenchymal Transition Generates Cellswithproperties of Stemcells. Cell 2008;133:704-15.
22. Floor S, van Staveren WC, Larsimont D, Dumont JE, Maenhaut C. Cancer cells in epithelial-to-mesenchymal transitionandtumor-propagating-cancer stemcells: distinct, overlapping or same populations. Oncogene 2011;30:4609-21.
23. Masamune A, Watanabe T, Kikuta K, Satoh K, Kanno A, Shimosegawa T. Nuclear expression of interleukin-33 in pancreatic stellate cells. Am J Physiol Gastrointest Liver Physiol 2010;299:G821-32.
24. Hong SP, Wen J, Bang S, Park S, Song SY. CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells. Int J Cancer 2009;125:2323-31.
25. PengS,ChenLL,LeiXX,YangL,LinH,CarmichaelGG,etal. Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells 2011;29:496-504.
26. Singh A, Wu H, Zhang P, Happel C, Ma J, Biswal S. Expression of ABCG2 (BCRP) is regulated by Nrf2 in cancer cells that confers side population and chemoresistance phenotype. Mol Cancer Ther 2010;9:2365-76.
27. Imai Y, Ohmori K, Yasuda S, Wada M, Suzuki T, Fukuda K, et al. Breast cancer resistance protein/ ABCG2 is differentially regulated downstream of extracellular signal-regulated kinase. Cancer Sci 2009;100:1118-27.
28. Bao B, Wang Z, Ali S, Kong D, Li Y, Ahmad A, et al. Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett 2011;307:26-36.
29. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83.
30. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97.
31. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-33.
32. Takikawa T, Masamune A, Hamada S, Nakano E, Yoshida N, Shimosegawa T. miR-210 regulates the interaction between pancreatic cancer cells and stellate cells. Biochem Biophys Res Commun 2013;437:433-9.
33. Bhardwaj A, Arora S, Prajapati VK, Singh S, Singh AP. Cancer "stemness"-regulating microRNAs: role, mechanisms and therapeutic potential. Curr Drug Targets 2013;14: 1175-84.
34. Ceppi P, Peter ME. MicroRNAs regulate both epithelialto-mesenchymal transition and cancer stem cells. Oncogene 2013; Epub ahead of print.
35. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One 2011;6:e24099.
36. Bao B, Wang Z, Ali S, Kong D, Banerjee S, Ahmad A, et al. Over-expression of FoxM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011;112:2296-306.
37. Okuda H, Xing F, Pandey PR, Sharma S, Watabe M, Pai SK, et al. miR-7 suppresses brain metastasis of breast cancer stem-like cells by modulating KLF4. Cancer Res 2013;73:1434-44.
38. Liu L, Dai Y, Chen J, Zeng T, Li Y, Chen L, et al. Maelstrom promotes hepatocellular carcinoma metastasis by inducing epithelial-mesenchymal transition via Akt/GSK-3b/snail signaling. Hepatology 2013; Epub ahead of print.