Human oral cancer cells with increasing tumorigenic abilities exhibit higher effective membrane capacitance

Integrative Biology (United Kingdom)

Volumn 6, Issue 5, 2014, Pages 545-554

  Liang, X ^a   Graham, K A ^b   Johannessen, A C ^a,c   Costea, D E ^a   Labeed, F H ^b  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; HYMECROMONE;

ADHERENT CELL; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CARCINOMA CELL; CELL MEMBRANE; CELL SURFACE; ELECTROPHORESIS; ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; MEMBRANE STRUCTURE; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY;

EID: 84899054343     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c3ib40255j     Document Type: Article

References (52)

1. A. I. Zavras A. J. Yoon M. K. Chen C. W. Lin S. F. Yang Metallothionein-1 genotypes in the risk of oral squamous cell carcinoma Ann. Surg. Oncol. 2011 18 1478 1483 10.1245/s10434-010-1431-3
2. L. Mao W. K. Hong V. A. Papadimitrakopoulou Focus on head and neck cancer Cancer Cell 2004 5 311 316 (Pubitemid 38482067)
3. B. M. Wensing M. A. Merkx P. F. Krabbe H. A. Marres F. J. Van den Hoogen Oral squamous cell carcinoma and a clinically negative neck: the value of follow-up Head Neck Oncol. 2011 33 1400 1405 10.1002/hed.21642
4. D. Bonnet J. E. Dick Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat. Med. 1997 3 730 737 (Pubitemid 27298715)
5. T. Reya S. J. Morrison M. F. Clarke I. L. Weissman Stem cells, cancer, and cancer stem cells Nature 2001 414 105 111 10.1038/35102167 (Pubitemid 33041634)
6. M. Al-Hajj M. S. Wicha A. Benito-Hernandez S. J. Morrison M. F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 2003 100 3983 3988 10.1073/pnas.0530291100 (Pubitemid 36418143)
7. C. Li D. G. Heidt P. Dalerba C. F. Burant L. Zhang V. Adsay M. Wicha M. F. Clarke D. M. Simeone Identification of pancreatic cancer stem cells Cancer Res. 2007 67 1030 1037 10.1158/0008-5472.CAN-06-2030
8. C. A. O'Brien A. Pollett S. Gallinger J. E. Dick A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 2007 445 106 110 10.1038/nature05372 (Pubitemid 46067310)
9. M. Locke M. Heywood S. Fawell I. C. Mackenzie Retention of intrinsic stem cell hierarchies in carcinoma-derived cell lines Cancer Res. 2005 65 8944 8950 10.1158/0008-5472.CAN-05-0931 (Pubitemid 41377385)
10. M. E. Prince R. Sivanandan A. Kaczorowski G. T. Wolf M. J. Kaplan P. Dalerba I. L. Weissman M. F. Clarke L. E. Ailles Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc. Natl. Acad. Sci. U. S. A. 2007 104 973 978 10.1073/pnas.0610117104 (Pubitemid 46154721)
11. L. J. Harper K. Piper J. Common F. Fortune I. C. Mackenzie Stem cell patterns in cell lines derived from head and neck squamous cell carcinoma J. Oral Pathol. Med. 2007 36 594 603 10.1111/j.1600-0714.2007.00617.x (Pubitemid 47609813)
12. L. J. Harper D. E. Costea L. Gammon B. Fazil A. Biddle I. C. Mackenzie Normal and malignant epithelial cells with stem-like properties have an extended G2 cell cycle phase that is associated with apoptotic resistance BMC Cancer 2010 10 166 10.1186/1471-2407-10-166
13. E. Quintana M. Shackleton M. S. Sabel D. R. Fullen T. M. Johnson S. J. Morrison Efficient tumour formation by single human melanoma cells Nature 2008 456 593 598 10.1038/nature07567
14. M. R. Alison S. Islam N. A. Wright Stem cells in cancer: instigators and propagators? J. Cell Sci. 2010 123 2357 2368 10.1242/jcs.054296
15. M. R. Clay M. Tabor J. H. Owen T. E. Carey C. R. Bradford G. T. Wolf M. S. Wicha M. E. Prince Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase Head Neck Oncol. 2010 32 1195 1201 10.1002/hed.21315
16. M. H. Tabor M. R. Clay J. H. Owen C. R. Bradford T. E. Carey G. T. Wolf M. E. Prince Head and neck cancer stem cells: the side population Laryngoscope 2011 121 527 533 10.1002/lary.21032
17. M. Shackleton E. Quintana Progress in understanding melanoma propagation Mol. Oncol. 2010 4 451 457 10.1016/j.molonc.2010.06.006
18. L. R. Strachan K. J. Scalapino H. J. Lawrence R. Ghadially Rapid adhesion to collagen isolates murine keratinocytes with limited long-term repopulating ability in vivo despite high clonogenicity in vitro Stem cells 2008 26 235 243 10.1634/stemcells.2007-0534
19. T. Igarashi S. Shimmura S. Yoshida M. Tonogi N. Shinozaki G. Y. Yamane Isolation of oral epithelial progenitors using collagen IV Oral Dis 2008 14 413 418 10.1111/j.1601-0825.2007.01390.x (Pubitemid 351841715)
20. S. E. Chang Y. Kim Pak H. W. Lee J. H. Choi E. J. Jeong S. H. Choi H. W. Chang Y. S. Chung S. Y. Kim Reduced mitochondrial properties in putative progenitor/stem cells of human keratinocytes Ann. Dermatol. 2009 21 364 368 10.5021/ad.2009.21.4.364
21. Z. Wu K. Shao G. Song Adhesion of hepatocellular carcinoma cells to collagen IV coated surfaces Zhonghua Heyixue Zazhi 1999 79 369 372
22. P. H. Jones F. M. Watt Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression Cell 1993 73 713 724 (Pubitemid 23159010)
23. H. A. Pohl, Dielectrophoresis, Cambridge University Press, Cambridge, 1978
24. M. P. Hughes, Nanoelectromechanics in Engineering and Biology, CRC Press, Boca Raton, 2002
25. T. B. Jones, Electromechanics of Particles, Cambridge University Press, Cambridge, 1995
26. L. M. Broche F. H. Labeed M. P. Hughes Extraction of dielectric properties of multiple populations from dielectrophoretic collection spectrum data Phys. Med. Biol. 2005 50 2267 2274 10.1088/0031-9155/50/10/006 (Pubitemid 40767815)
27. H. A. Pohl I. Hawk Separation of living and dead cells by dielectrophoresis Science 1966 152 647 649 10.1126/science.152.3722.647-a
28. F. H. Labeed H. M. Coley H. Thomas M. P. Hughes Assessment of multidrug resistance reversal using dielectrophoresis and flow cytometry Biophys. J. 2003 85 2028 2034 10.1016/S0006-3495(03)74630-X (Pubitemid 37052282)
29. F. Yang X. Yang H. Jiang P. Bulkhaults P. Wood W. Hrushesky G. Wang Dielectrophoretic separation of colorectal cancer cells Biomicrofluidics 2010 4 13204 10.1063/1.3279786
30. P. R. Gascoyne X. B. Wang Y. Huang F. F. Becker Dielectrophoretic Separation of Cancer Cells from Blood IEEE Trans. Ind. Appl. 1997 33 670 678 10.1109/28.585856 (Pubitemid 127828225)
31. L. A. Flanagan J. Lu L. Wang S. A. Marchenko N. L. Jeon A. P. Lee E. S. Monuki Unique dielectric properties distinguish stem cells and their differentiated progeny Stem cells 2008 26 656 665 10.1634/stemcells.2007-0810
32. A. Salmanzadeh E. S. Elvington P. C. Roberts E. M. Schmelz R. V. Davalos Sphingolipid metabolites modulate dielectric characteristics of cells in a mouse ovarian cancer progression model Integr. Biol. 2013 5 843 852 10.1039/c3ib00008g
33. H. J. Mulhall F. H. Labeed B. Kazmi D. E. Costea M. P. Hughes M. P. Lewis Cancer, pre-cancer and normal oral cells distinguished by dielectrophoresis Anal. Bioanal. Chem. 2011 401 2455 2463 10.1007/s00216-011-5337-0
34. S. E. Chang S. Foster D. Betts W. E. Marnock DOK, a cell line established from human dysplastic oral mucosa, shows a partially transformed non-malignant phenotype Int. J. Cancer 1992 52 896 902 (Pubitemid 23009506)
35. S. S. Prime S. V. Nixon I. J. Crane A. Stone J. B. Matthews N. J. Maitland L. Remnant S. K. Powell S. M. Game C. Scully The behaviour of human oral squamous cell carcinoma in cell culture J. Pathol. 1990 160 259 269 10.1002/path.1711600313 (Pubitemid 20115509)
36. D. Sapkota D. E. Costea M. Blo O. Bruland J. B. Lorens E. N. Vasstrand S. O. Ibrahim S100A14 inhibits proliferation of oral carcinoma derived cells through G1-arrest Oral Oncol. 2012 48 219 225 10.1016/j.oraloncology.2011.10.001
37. D. E. Costea A. O. Dimba L. L. Loro O. K. Vintermyr A. C. Johannessen The phenotype of in vitro reconstituted normal human oral epithelium is essentially determined by culture medium J. Oral Pathol. Med. 2005 34 247 252 10.1111/j.1600-0714.2005.00308.x (Pubitemid 40445159)
38. D. E. Costea L. L. Loro E. A. Dimba O. K. Vintermyr A. C. Johannessen Crucial effects of fibroblasts and keratinocyte growth factor on morphogenesis of reconstituted human oral epithelium J. Invest. Dermatol. 2003 121 1479 1486 10.1111/j.1523-1747.2003.12616.x (Pubitemid 38005502)
39. F. H. Labeed H. M. Coley M. P. Hughes Differences in the biophysical properties of membrane and cytoplasm of apoptotic cells revealed using dielectrophoresis Biochim. Biophys. Acta 2006 1760 922 929 10.1016/j.bbagen. 2006.01.018 (Pubitemid 43816174)
40. K. F. Hoettges Y. Hubner L. M. Broche S. L. Ogin G. E. Kass M. P. Hughes Dielectrophoresis-activated multiwell plate for label-free high-throughput drug assessment Anal. Chem. 2008 80 2063 2068 10.1021/ac702083g (Pubitemid 351458053)
41. D. S. Kim H. J. Cho H. R. Choi S. B. Kwon K. C. Park Isolation of human epidermal stem cells by adherence and the reconstruction of skin equivalents Cell. Mol. Life Sci. 2004 61 2774 27281 10.1007/s00018-004-4288-4 (Pubitemid 40022441)
42. D. K. Lieu L. A. Degraffenried R. R. Isseroff E. A. Kurzrock Beta1 integrin expression pattern in transitional urothelium does not allow for efficient stem cell enrichment as in other epithelia Tissue Eng. 2007 13 263 270 10.1089/ten.2006.0132
43. S. P. Desai M. D. Vahey J. Voldman Electrically addressable vesicles: tools for dielectrophoresis metrology Langmuir 2009 25 3867 3875 10.1021/la803330c
44. G. Teti C. Cavallo B. Grigolo S. Giannini A. Facchini A. Mazzotti M. Falconi Ultrastructural analysis of human bone marrow mesenchymal stem cells during in vitro osteogenesis and chondrogenesis Microsc. Res. Tech. 2012 75 596 604 10.1002/jemt.21096
45. A. M. Marzesco P. Janich M. Wilsch-Brauninger V. Dubreuil K. Langenfeld D. Corbeil W. B. Huttner Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells J. Cell Sci. 2005 118 2849 2858 10.1242/jcs.02439 (Pubitemid 41136362)
46. A. Ruiz i Altaba V. Palma N. Dahmane Hedgehog-Gli signalling and the growth of the brain Nat. Rev. Neurosci. 2002 3 24 33 10.1038/nrn704 (Pubitemid 135706562)
47. D. Corbeil K. Roper A. Hellwig M. Tavian S. Miraglia S. M. Watt P. J. Simmons B. Peault D. W. Buck W. B. Huttner The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions J. Biol. Chem. 2000 275 5512 5520 (Pubitemid 30115186)
48. E. J. Hagedorn H. Yashiro J. W. Ziel S. Ihara Z. Wang D. R. Sherwood Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans Dev. Cell 2009 17 187 198 10.1016/j.devcel.2009.06.006
49. S. A. Mani W. Guo M. J. Liao E. N. Eaton A. Ayyanan A. Y. Zhou M. Brooks F. Reinhard C. C. Zhang M. Shipitsin L. L. Campbell K. Polyak C. Brisken J. Yang R. A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 2008 133 704 715 10.1016/j.cell.2008.03.027 (Pubitemid 351636299)
50. A. Biddle I. C. Mackenzie Cancer stem cells and EMT in carcinoma Cancer Metastasis Rev. 2012 31 10.1007/s10555-012-9345-0
51. F. H. Labeed J. Lu H. J. Mulhall S. A. Marchenko K. F. Hoettges L. C. Estrada A. P. Lee M. P. Hughes L. A. Flanagan Biophysical characteristics reveal neural stem cell differentiation potential PLoS One 2011 6 e25458 10.1371/journal.pone.0025458
52. (Pubitemid 40372904)