Anchorage-dependent multicellular aggregate formation induces CD44 high cancer stem cell-like ATL cells in an NF-κB- and vimentin-dependent manner

Cancer Letters

Volumn 357, Issue 1, 2015, Pages 355-363

  Miyatake, Yukiko ^a,b   Sheehy, Noreen ^b   Ikeshita, Shunji ^a   Hall, William W ^b   Kasahara, Masanori ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cancer stem cells; CD44; Coculture; Vimentin, ATL

Indexed keywords

CD44V9 ANTIGEN; CYTOSKELETON PROTEIN; HERMES ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; UNCLASSIFIED DRUG; VIMENTIN; WITHAFERIN A; CD44 PROTEIN, HUMAN;

ANCHORAGE DEPENDENT MULTICELLULAR AGGREGATE; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CELL AGGREGATION; CELL ANCHORAGE; CELL COUNT; CELL FRACTIONATION; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEEDER CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKEMIA CELL; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPSE; T CELL LEUKEMIA; APOPTOSIS; HEK293 CELL LINE; JURKAT CELL LINE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE;

ANTIGENS, CD44; APOPTOSIS; HEK293 CELLS; HUMANS; JURKAT CELLS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; NEOPLASTIC STEM CELLS; NF-KAPPA B; TUMOR CELLS, CULTURED; VIMENTIN;

EID: 84920368901     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.11.055     Document Type: Article

References (47)

1. Poiesz B.J., Ruscetti F.W., Gazdar A.F., Bunn P.A., Minna J.D., Gallo R.C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. U.S.A. 1980, 77:7415-7419.
2. Bittencourt A.L., de Oliveira Mde F. Cutaneous manifestations associated with HTLV-1 infection. Int. J. Dermatol 2010, 49:1099-1110.
3. Ohshima K. Pathological features of diseases associated with human T-cell leukemia virus type I. Cancer Sci 2007, 98:772-778.
4. Nasr R., El Hajj H., Kfoury Y., de Thé H., Hermine O., Bazarbachi A. Controversies in targeted therapy of adult T cell leukemia/lymphoma: ON target or OFF target effects?. Viruses 2011, 3:750-769.
5. Tsukasaki K., Hermine O., Bazarbachi A., Ratner L., Ramos J.C., Harrington W., et al. Definition, prognostic factors, treatment, and response criteria of adult T-cell leukemia-lymphoma: a proposal from an international consensus meeting. J. Clin. Oncol 2009, 27:453-459.
6. Tsutsumi Y., Shimono J., Miyashita N., Teshima T. No effect of humanized CCR monoclonal antibody (mogamulizumab) on treatment-resistant adult T cell leukemia with meningeal infiltration. Leuk. Lymphoma 2014, 55:457-459.
7. Huntly B.J., Gilliland D.G. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat. Rev. Cancer 2005, 5:311-321.
8. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
9. Zöller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat. Rev. Cancer 2011, 11:254-267.
10. Su Y.J., Lai H.M., Chang Y.W., Chen G.Y., Lee J.L. Direct reprogramming of stem cell properties in colon cancer cells by CD44. EMBO J. 2011, 30:3186-3199.
11. Ishimoto T., Nagano O., Yae T., Tamada M., Motohara T., Oshima H., et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 2011, 19:387-400.
12. Chagan-Yasutan H., Tsukasaki K., Takahashi Y., Oguma S., Harigae H., Ishii N., et al. Involvement of osteopontin and its signaling molecule CD44 in clinicopathological features of adult T cell leukemia. Leuk. Res 2011, 35:1484-1490.
13. Huber M.A., Azoitei N., Baumann B., Grünert S., Sommer A., Pehamberger H., et al. NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J. Clin. Invest 2004, 114:569-581.
14. Bourguignon L.Y., Peyrollier K., Xia W., Gilad E. Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J. Biol. Chem 2008, 283:17635-17651.
15. Hinohara K., Kobayashi S., Kanauchi H., Shimizu S., Nishioka K., Tsuji E., et al. ErbB receptor tyrosine kinase/NF-κB signaling controls mammosphere formation in human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6584-6589.
16. Zhou J., Zhang H., Gu P., Bai J., Margolick J.B., Zhang Y. NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res. Treat 2008, 111:419-427.
17. Mori N., Fujii M., Ikeda S., Yamada Y., Tomonaga M., Ballard D.W., et al. Constitutive activation of NF-kappaB in primary adult T-cell leukemia cells. Blood 1999, 93:2360-2368.
18. Hironaka N., Mochida K., Mori N., Maeda M., Yamamoto N., Yamaoka S. Tax-independent constitutive IkappaB kinase activation in adult T-cell leukemia cells. Neoplasia 2004, 6:266-278.
19. Borovski T., De Sousa F., Melo E., Vermeulen L., Medema J.P. Cancer stem cell niche: the place to be. Cancer Res 2011, 71:634-639.
20. Li L., Neaves W.B. Normal stem cells and cancer stem cells: the niche matters. Cancer Res 2006, 66:4553-4557.
21. Solis M.A., Chen Y.H., Wong T.Y., Bittencourt V.Z., Lin Y.C., Huang L.L. Hyaluronan regulates cell behavior: a potential niche matrix for stem cells. Biochem. Res. Int 2012, 2012:346972.
22. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
23. Havasi P., Nabioni M., Soleimani M., Bakhshandeh B., Parivar K. Mesenchymal stem cells as an appropriate feeder layer for prolonged in vitro culture of human induced pluripotent stem cells. Mol. Biol. Rep 2013, 40:3023-3031.
24. Hovatta O., Mikkola M., Gertow K., Strömberg A.M., Inzunza J., Hreinsson J., et al. A culture system using human foreskin fibroblasts as feeder cells allows production of human embryonic stem cells. Hum. Reprod 2003, 18:1404-1409.
25. Takahashi K., Narita M., Yokura M., Ichisaka T., Yamanaka S. Human induced pluripotent stem cells on autologous feeders. PLoS ONE 2009, 4:e8067.
26. Catalina P., Montes R., Ligero G., Sanchez L., de la Cueva T., Bueno C., et al. Human ESCs predisposition to karyotypic instability: is a matter of culture adaptation or differential vulnerability among hESC lines due to inherent properties?. Mol. Cancer 2008, 7:76.
27. Draper J.S., Smith K., Gokhale P., Moore H.D., Maltby E., Johnson J., et al. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol 2004, 22:53-54.
28. Miyatake Y., Oliveira A.L., Jarboui M.A., Ota S., Tomaru U., Teshima T., et al. Protective roles of epithelial cells in the survival of adult T-cell leukemia/lymphoma cells. Am. J. Pathol 2013, 182:1832-1842.
29. Wayner E.A., Gil S.G., Murphy G.F., Wilke M.S., Carter W.G. Epiligrin, a component of epithelial basement membranes, is an adhesive ligand for alpha 3 beta 1 positive T lymphocytes. J. Cell Biol 1993, 121:1141-1152.
30. Grin B., Mahammad S., Wedig T., Cleland M.M., Tsai L., Herrmann H., et al. Withaferin a alters intermediate filament organization, cell shape and behavior. PLoS ONE 2012, 7:e39065.
31. Miyatake Y., Ikeda H., Ishizu A., Baba T., Ichihashi T., Suzuki A., et al. Role of neuronal interferon-gamma in the development of myelopathy in rats infected with human T-cell leukemia virus type 1. Am. J. Pathol 2006, 169:189-199.
32. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
33. Wang Z., Oron E., Nelson B., Razis S., Ivanova N. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell 2012, 10:440-454.
34. Bentires-Alj M., Barbu V., Fillet M., Chariot A., Relic B., Jacobs N., et al. NF-kappaB transcription factor induces drug resistance through MDR1 expression in cancer cells. Oncogene 2003, 22:90-97.
35. Vanden Berghe W., Sabbe L., Kaileh M., Haegeman G., Heyninck K. Molecular insight in the multifunctional activities of withaferin A. Biochem. Pharmacol 2012, 84:1282-1291.
36. Yang Z., Garcia A., Xu S., Powell D.R., Vertino P.M., Singh S., et al. Withania somnifera root extract inhibits mammary cancer metastasis and epithelial to mesenchymal transition. PLoS ONE 2013, 8:e75069.
37. Bargagna-Mohan P., Hamza A., Kim Y.E., Khuan Abby Ho Y., Mor-Vaknin N., Wendschlag N., et al. The tumor inhibitor and antiangiogenic agent withaferin A targets the intermediate filament protein vimentin. Chem. Biol 2007, 14:623-634.
38. Lahat G., Zhu Q.S., Huang K.L., Wang S., Bolshakov S., Liu J., et al. Vimentin is a novel anti-cancer therapeutic target; insights from in vitro and in vivo mice xenograft studies. PLoS ONE 2010, 5:e10105.
39. Satelli A., Li S. Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell. Mol. Life Sci 2011, 68:3033-3046.
40. Marks P.A., Richon V.M., Rifkind R.A. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst 2000, 92:1210-1216.
41. West A.C., Johnstone R.W. New and emerging HDAC inhibitors for cancer treatment. J. Clin. Invest 2014, 124:30-39.
42. Mann B.S., Johnson J.R., Cohen M.H., Justice R., Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 2007, 12:1247-1252.
43. Olsen E.A., Kim Y.H., Kuzel T.M., Pacheco T.R., Foss F.M., Parker S., et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J. Clin. Oncol 2007, 25:3109-3115.
44. Piekarz R.L., Frye R., Prince H.M., Kirschbaum M.H., Zain J., Allen S.L., et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood 2011, 117:5827-5834.
45. Hudson L.G., Zeineldin R., Stack M.S. Phenotypic plasticity of neoplastic ovarian epithelium: unique cadherin profiles in tumor progression. Clin. Exp. Metastasis 2008, 25:643-655.
46. Gravelle P., Jean C., Familiades J., Decaup E., Blanc A., Bezombes-Cagnac C., et al. Cell growth in aggregates determines gene expression, proliferation, survival, chemoresistance, and sensitivity to immune effectors in follicular lymphoma. Am. J. Pathol 2014, 184:282-295.
47. Gérard A., Khan O., Beemiller P., Oswald E., Hu J., Matloubian M., et al. Secondary T cell-T cell synaptic interactions drive the differentiation of protective CD8+ T cells. Nat. Immunol 2013, 14:356-363.