Journal of Hepatology
Volume 54, Issue 1 , Pages 122-131 , January 2011

Dysadherin can enhance tumorigenesis by conferring properties of stem-like cells to hepatocellular carcinoma cells

  • Jeong-Ran Park

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • These authors contributed equally to this work.
    • ,
  • Ran-Ju Kim

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • These authors contributed equally to this work.
    • ,
  • Yoo-Kyung Lee

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • ,
  • Soo-Rim Kim

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • ,
  • Kyung-Jin Roh

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • ,
  • Seung Hyun Oh

      Affiliations

    • Division of Cancer Biology, National Cancer Center, Goyang, South Korea
    • ,
  • Gu Kong

      Affiliations

    • Department of Pathology, College of Medicine, Hanyang University, Seoul, South Korea
    • ,
  • Kyung-Sun Kang

      Affiliations

    • Laboratory of Stem Cell and Tumor Biology, Department of Veterinary Public Health, College of Veterinary Medicine, Seoul National University, Seoul, South Korea
    • ,
  • Jeong-Seok Nam

      Affiliations

    • Laboratory of Tumor Suppressor, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, South Korea
    • Corresponding Author InformationCorresponding author. Tel./fax: +82 32 899 6072/6350.

Received 10 March 2010 ,Revised 27 May 2010 ,Accepted 2 June 2010.

References 

  1. Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer. 2006;6:674–687
  2. Lee TK, Castilho A, Ma S, Ng IO. Liver cancer stem cells: implications for a new therapeutic target. Liver Int. 2009;29:955–965
  3. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality?. Nat Med. 2009;15:1010–1012
  4. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983–3988
  5. Patrawala L, Calhoun-Davis T, Schneider-Broussard R, Tang DG. Hierarchical organization of prostate cancer cells in xenograft tumors: the CD44+alpha2beta1+ cell population is enriched in tumor-initiating cells. Cancer Res. 2007;67:6796–6805
  6. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A. 2007;104:10158–10163
  7. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology. 2006;44:240–251
  8. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–824
  9. Salnikov AV, Kusumawidjaja G, Rausch V, Bruns H, Gross W, Khamidjanov A, et al. Cancer stem cell marker expression in hepatocellular carcinoma and liver metastases is not sufficient as single prognostic parameter. Cancer Lett. 2009;275:185–193
  10. Wang J, Sakariassen PO, Tsinkalovsky O, Immervoll H, Boe SO, Svendsen A, et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer. 2008;122:761–768
  11. Ino Y, Gotoh M, Sakamoto M, Tsukagoshi K, Hirohashi S. Dysadherin, a cancer-associated cell membrane glycoprotein, down-regulates E-cadherin and promotes metastasis. Proc Natl Acad Sci U S A. 2002;99:365–370
  12. Nam JS, Hirohashi S, Wakefield LM. Dysadherin: a new player in cancer progression. Cancer Lett. 2007;255:161–169
  13. Kim RJ, Kim SR, Roh KJ, Park SB, Park JR, Kang KS, et al. Ras activation contributes to the maintenance and expansion of Sca-1pos cells in a mouse model of breast cancer. Cancer Lett. 2010;287:172–181
  14. Park JR, Jung JW, Seo MS, Kang SK, Lee YS, Kang KS. DNER modulates adipogenesis of human adipose tissue-derived mesenchymal stem cells via regulation of cell proliferation. Cell prolif. 2010;43:19–28
  15. Shimamura T, Yasuda J, Ino Y, Gotoh M, Tsuchiya A, Nakajima A, et al. Dysadherin expression facilitates cell motility and metastatic potential of human pancreatic cancer cells. Cancer Res. 2004;64:6989–6995
  16. Wurmbach E, Chen YB, Khitrov G, Zhang W, Roayaie S, Schwartz M, et al. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma. Hepatology. 2007;45:938–947
  17. Libbrecht L. Hepatic progenitor cells in human liver tumor development. World J Gastroenterol. 2006;12:6261–6265
  18. Matsui J, Wakabayashi T, Asada M, Yoshimatsu K, Okada M. Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J Biol Chem. 2004;279:18600–18607
  19. Carlin R, Davis D, Weiss M, Schultz B, Troyer D. Expression of early transcription factors Oct-4, Sox-2 and Nanog by porcine umbilical cord (PUC) matrix cells. Reprod Biol Endocrinol. 2006;4:8
  20. Dallas NA, Xia L, Fan F, Gray MJ, Gaur P, van Buren G, et al. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res. 2009;69:1951–1957
  21. Sanchez-Partida LG, Simerly CR, Ramalho-Santos J. Freeze-dried primate sperm retains early reproductive potential after intracytoplasmic sperm injection. Fertil Steril. 2008;89:742–745
  22. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, et al. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A. 2004;101:14228–14233
  23. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science. 2002;298:597–600
  24. Islam MO, Kanemura Y, Tajria J, Mori H, Kobayashi S, Shofuda T, et al. Characterization of ABC transporter ABCB1 expressed in human neural stem/progenitor cells. FEBS Lett. 2005;579:3473–3480
  25. Sanchez PV, Perry RL, Sarry JE, Perl AE, Murphy K, Swider CR, et al. A robust xenotransplantation model for acute myeloid leukemia. Leukemia. 2009;23:2109–2117
  26. Ueda K, Cardarelli C, Gottesman MM, Pastan I. Expression of a full-length cDNA for the human “MDR1” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci U S A. 1987;84:3004–3008
  27. Gyorffy B, Surowiak P, Kiesslich O, Denkert C, Schafer R, Dietel M, et al. Gene expression profiling of 30 cancer cell lines predicts resistance towards 11 anticancer drugs at clinically achieved concentrations. Int J Cancer. 2006;118:1699–1712
  28. Bunting KD, Zhou S, Lu T, Sorrentino BP. Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood. 2000;96:902–909
  29. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755–768
  30. Norwood K, Wang RY, Hirschmann-Jax C, Andreeff M, Brenner MK, Goodell MA, et al. An in vivo propagated human acute myeloid leukemia expressing ABCA3. Leuk Res. 2004;28:295–299
  31. Hirohashi S, Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci. 2003;94:575–581
  32. Brabletz T, Hlubek F, Spaderna S, Schmalhofer O, Hiendlmeyer E, Jung A, et al. Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and beta-catenin. Cells Tissues Organs. 2005;179:56–65
  33. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–715
  34. Karpowicz P, Willaime-Morawek S, Balenci L, DeVeale B, Inoue T, van der Kooy D. E-Cadherin regulates neural stem cell self-renewal. J Neurosci. 2009;29:3885–3896
  35. Shook D, Keller R. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech Dev. 2003;120:1351–1383
  36. Garty H, Karlish SJ. Role of FXYD proteins in ion transport. Annu Rev Physiol. 2006;68:431–459
  37. Rajasekaran SA, Rajasekaran AK. Na, K-ATPase and epithelial tight junctions. Front Biosci. 2009;14:2130–2148
  38. Shin K, Fogg VC, Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol. 2006;22:207–235
  39. Nagamatsu G, Ohmura M, Mizukami T, Hamaguchi I, Hirabayashi S, Yoshida S, et al. A CTX family cell adhesion molecule, JAM4, is expressed in stem cell and progenitor cell populations of both male germ cell and hematopoietic cell lineages. Mol Cell Biol. 2006;26:8498–8506
  40. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–659

PII: S0168-8278(10)00716-6

doi: 10.1016/j.jhep.2010.06.026

Journal of Hepatology
Volume 54, Issue 1 , Pages 122-131 , January 2011

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