Identification of a population of epidermal squamous cell carcinoma cells with enhanced potential for tumor formation

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Adhikary, Gautam ^a   Grun, Dan ^a   Kerr, Candace ^a   Balasubramanian, Sivaprakasam ^a   Rorke, Ellen A ^a   Vemuri, Mohan ^b   Boucher, Shayne ^b   Bickenbach, Jackie R ^c   Hornyak, Thomas ^a   Xu, Wen ^a   Fisher, Matthew L ^a   Eckert, Richard L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Life Technologies Inc   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BMI1 PROTEIN; CD200 ANTIGEN; CYTOKERATIN 15; CYTOKERATIN 19; HISTONE H3; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CARCINOGENESIS; CELL GROWTH; CELL POPULATION; EPIDERMAL SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SKIN CARCINOMA; SPHEROID CELL; SQUAMOUS CELL CARCINOMA; STEM CELL; TUMOR GROWTH; TUMOR SPHEROID; TUMOR VOLUME;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL CULTURE TECHNIQUES; CELL TRANSFORMATION, NEOPLASTIC; EPIDERMIS; HUMANS; IMMUNOBLOTTING; MICE; NEOPLASTIC STEM CELLS; SPHEROIDS, CELLULAR; TUMOR MARKERS, BIOLOGICAL;

EID: 84893438154     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084324     Document Type: Article

References (64)

1. Gupta S, Mukhtar H (2002) Chemoprevention of skin cancer: current status and future prospects. Cancer Metastasis Rev 21: 363-380. doi: 10.1023/A:1021275330385. PubMed: 12549772. (Pubitemid 36071921)
2. Pincelli C, Marconi A (2010) Keratinocyte stem cells: friends and foes. J Cell Physiol 225: 310-315. doi:10.1002/jcp.22275. PubMed: 20568222.
3. Al-Hajj M, Clarke MF (2004) Self-renewal and solid tumor stem cells. Oncogene 23: 7274-7282. doi:10.1038/sj.onc.1207947. PubMed: 15378087. (Pubitemid 39382161)
4. Al-Hajj M, Wicha MS, ito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988 (Pubitemid 36418143)
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J et al. (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401. doi:10.1038/nature03128. PubMed: 15549107. (Pubitemid 39551674)
6. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828. PubMed: 14522905. (Pubitemid 37187480)
7. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110. doi:10.1038/nature05372. PubMed: 17122772. (Pubitemid 46067310)
8. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323. doi:10.1016/j.stem.2007.06.002. PubMed: 18371365. (Pubitemid 47355323)
9. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ et al. (2007) 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 104: 973-978. doi:10.1073/pnas.0610117104. PubMed: 17210912. (Pubitemid 46154721)
10. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G et al. (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389. doi:10.1158/0008-5472.CAN-08-4418. PubMed: 19336570.
11. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI et al. (2009) Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 385: 307-313. doi:10.1016/j.bbrc. 2009.05.048. PubMed: 19450560.
12. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J et al. (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7: 330-338. doi:10.1158/1541-7786.MCR-08-0393. PubMed: 19276181.
13. Ma S, Chan KW, Lee TK, Tang KH, Wo JY et al. (2008) Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 6: 1146-1153. doi:10.1158/1541-7786.MCR-08-0035. PubMed: 18644979.
14. Inoue K, Aoi N, Sato T, Yamauchi Y, Suga H et al. (2009) Differential expression of stem-cell-associated markers in human hair follicle epithelial cells. Lab Invest 89: 844-856. doi:10.1038/labinvest.2009.48. PubMed: 19506554.
15. Li A, Simmons PJ, Kaur P (1998) Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci U S A 95: 3902-3907. doi:10.1073/pnas.95.7.3902. PubMed: 9520465. (Pubitemid 28173226)
16. Jones PH, Watt FM (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73: 713-724. doi:10.1016/0092-8674(93)90251-K. PubMed: 8500165. (Pubitemid 23159010)
17. Patel GK, Yee CL, Terunuma A, Telford WG, Voong N et al. (2012) Identification and characterization of tumor-initiating cells in human primary cutaneous squamous cell carcinoma. J Invest Dermatol 132: 401-409. doi:10.1038/jid.2011.317. PubMed: 22011906.
18. Patel GK, Yee CL, Yuspa SH, Vogel JC (2012) A humanized stromal bed is required for engraftment of isolated human primary squamous cell carcinoma cells in immunocompromised mice. J Invest Dermatol 132: 284-290. doi:10.1038/jid. 2011.284. PubMed: 21975825.
19. Eckert RL, Adhikary G, Balasubramanian S, Rorke EA, Vemuri MC et al. (2013) Biochemistry of epidermal stem cells. Biochim Biophys Acta 1830: 2427-2434. doi:10.1016/j.bbagen.2012.07.002. PubMed: 22820019.
20. López J, Poitevin A, Mendoza-Martínez V, Pérez-Plasencia C, García- Carrancá A (2012) Cancer-initiating cells derived from established cervical cell lines exhibit stem-cell markers and increased radioresistance. BMC Cancer 12: 48. doi:10.1186/1471-2407-12-48. PubMed: 22284662.
21. Mancini R, Giarnieri E, De VC, Malanga D, Roscilli G et al. (2011) Spheres derived from lung adenocarcinoma pleural effusions: molecular characterization and tumor engraftment. PLOS ONE 6: e21320. doi:10.1371/journal. pone.0021320. PubMed: 21789168.
22. Dontu G, Wicha MS (2005) Survival of mammary stem cells in suspension culture: implications for stem cell biology and neoplasia. J Mammary Gland Biol Neoplasia 10: 75-86. doi:10.1007/s10911-005-2542-5. PubMed: 15886888. (Pubitemid 40724024)
23. Liu S, Dontu G, Wicha MS (2005) Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res 7: 86-95. doi: 10.1186/bcr1021. PubMed: 15987436. (Pubitemid 40704127)
24. Eckert RL, Adhikary G, Rorke EA, Chew YC, Balasubramanian S (2011) Polycomb group proteins are key regulators of keratinocyte function. J Invest Dermatol 131: 295-301. doi:10.1038/jid.2010.318. PubMed: 21085188.
25. Grimaud C, Nègre N, Cavalli G (2006) From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res 14: 363-375. doi:10.1007/s10577-006-1069-y. PubMed: 16821133.
26. Levine SS, King IF, Kingston RE (2004) Division of labor in polycomb group repression. Trends Biochem Sci 29: 478-485. doi:10.1016/j.tibs. 2004.07.007. PubMed: 15337121.
27. Chen C, Wei Y, Hummel M, Hoffmann TK, Gross M et al. (2011) Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLOS ONE 6: e16466. doi:10.1371/journal.pone.0016466. PubMed: 21304586.
28. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567. doi:10.1016/j.stem.2007.08.014. PubMed: 18371393. (Pubitemid 350056407)
29. Zhang G, Ma L, Xie YK, Miao XB, Jin C (2012) Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity. Mol Med Report 6: 519-524
30. Calenic B, Ishkitiev N, Yaegaki K, Imai T, Costache M et al. (2010) Characterization of oral keratinocyte stem cells and prospects of its differentiation to oral epithelial equivalents. Rom J Morphol Embryol 51: 641-645. PubMed: 21103620.
31. Clevers H (2011) The cancer stem cell: premises, promises and challenges. Nat Med 17: 313-319. PubMed: 21386835.
32. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344. doi:10.1158/0008-5472.CAN-06- 3126. PubMed: 16990346.
33. Singh A, Park H, Kangsamaksin T, Singh A, Readio N et al. (2012) Keratinocyte Stem Cells and the Targets for Nonmelanoma Skin Cancer. Photochem Photobiol, 88: 1099-110. PubMed: 22211846.
34. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507. doi:10.1038/ng.127. PubMed: 18443585. (Pubitemid 351601215)
35. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ et al. (2011) Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 71: 5317-5326. doi:10.1158/0008-5472.CAN-11-1059. PubMed: 21685475.
36. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ et al. (2008) Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and highgrade oral squamous cell carcinoma. Clin Cancer Res 14: 4085-4095. doi:10.1158/1078-0432.CCR-07-4404. PubMed: 18593985.
37. Gu G, Yuan J, Wills M, Kasper S (2007) Prostate cancer cells with stem cell characteristics reconstitute the original human tumor in vivo. Cancer Res 67: 4807-4815. doi:10.1158/0008-5472.CAN-06-4608. PubMed: 17510410. (Pubitemid 46910189)
38. Liu A, Yu X, Liu S (2013) Pluripotency transcription factors and cancer stem cells: small genes make a big difference. Chin J Cancer, 32: 483-7. PubMed: 23419197.
39. Tai MH, Chang CC, Kiupel M, Webster JD, Olson LK et al. (2005) Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502. PubMed: 15513931. (Pubitemid 40246573)
40. Mills AA (2010) Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 10: 669-682. doi: 10.1038/nrc2931. PubMed: 20865010.
41. Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10: 697-708. doi:10.1038/nrn2731. PubMed: 19738629.
42. Pasini D, Bracken AP, Jensen MR, Lazzerini DE, Helin K (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061-4071. doi:10.1038/sj.emboj.7600402. PubMed: 15385962. (Pubitemid 39472427)
43. Li Z, Cao R, Wang M, Myers MP, Zhang Y et al. (2006) Structure of a Bmi-1-Ring1B polycomb group ubiquitin ligase complex. J Biol Chem 281: 20643-20649. doi:10.1074/jbc.M602461200. PubMed: 16714294. (Pubitemid 44065835)
44. Balasubramanian S, Lee K, Adhikary G, Gopalakrishnan R, Rorke EA et al. (2008) The Bmi-1 polycomb group gene in skin cancer: regulation of function by (-)-epigallocatechin-3-gallate. Nutr Rev 66 Suppl 1: S65-S68. doi:10.1111/j.1753-4887.2007.00009.x. PubMed: 18673494.
45. Balasubramanian S, Adhikary G, Eckert RL (2010) The Bmi-1 polycomb protein antagonizes the (-)-epigallocatechin-3-gallatedependent suppression of skin cancer cell survival. Carcinogenesis 31: 496-503. doi:10.1093/carcin/ bgp314. PubMed: 20015867.
46. Balasubramanian S, Chew YC, Eckert RL (2011) Sulforaphane Suppresses Polycomb Group Protein Level via a Proteasome- Dependent Mechanism in Skin Cancer Cells. Mol Pharmacol 80: 870-878. doi:10.1124/mol.111.072363. PubMed: 21807989.
47. Balasubramanian S, Kanade S, Han B, Eckert RL (2012) A proteasome inhibitor-stimulated Nrf1-dependent compensatory increase in proteasome subunit gene expression reduces polycomb group protein level. J Biol Chem 287: 36179-36189. doi:10.1074/jbc.M112.359281. PubMed: 22932898.
48. Choudhury SR, Balasubramanian S, Chew YC, Han B, Marquez VE et al. (2011) (-)-Epigallocatechin-3-gallate and DZNep reduce polycomb protein level via a proteasome-dependent mechanism in skin cancer cells. Carcinogenesis 32: 1525-1532. doi:10.1093/carcin/bgr171. PubMed: 21798853.
49. Suvà ML, Riggi N, Janiszewska M, Radovanovic I, Provero P et al. (2009) EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 69: 9211-9218. doi:10.1158/0008-5472.CAN-09-1622. PubMed: 19934320.
50. Kong D, Heath E, Chen W, Cher ML, Powell I et al. (2012) Loss of Let-7 Up-Regulates EZH2 in Prostate Cancer Consistent with the Acquisition of Cancer Stem Cell Signatures That Are Attenuated by BRDIM. PLOS ONE 7: e33729. doi:10.1371/journal.pone.0033729. PubMed: 22442719.
51. Changchien YC, Tátrai P, Papp G, Sápi J, Fónyad L et al. (2012) Poorly differentiated synovial sarcoma is associated with high expression of enhancer of zeste homologue 2 (EZH2). J Transl Med 10: 216. doi:10.1186/1479-5876-10-216. PubMed: 23110793.
52. Ott M, Litzenburger UM, Sahm F, Rauschenbach KJ, Tudoran R et al. (2012) Promotion of Glioblastoma Cell Motility by Enhancer of Zeste Homolog 2 (EZH2) Is Mediated by AXL Receptor Kinase. PLOS ONE 7: e47663. doi:10.1371/journal.pone. 0047663. PubMed: 23077658.
53. Crea F, Fornaro L, Bocci G, Sun L, Farrar WL et al. (2012) EZH2 inhibition: targeting the crossroad of tumor invasion and angiogenesis. Cancer Metastasis Rev 31: 753-761. doi:10.1007/s10555-012-9387-3. PubMed: 22711031.
54. Simon JA, Lange CA (2008) Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 647: 21-29. doi:10.1016/j.mrfmmm.2008.07.010. PubMed: 18723033.
55. Richardson PG, Sonneveld P, Schuster MW, Irwin D, Stadtmauer EA et al. (2005) Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 352: 2487-2498. doi:10.1056/NEJMoa043445. PubMed: 15958804. (Pubitemid 41007864)
56. Knutson SK, Wigle TJ, Warholic NM, Sneeringer CJ, Allain CJ et al. (2012) A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat Chem Biol 8: 890-896. PubMed: 23023262.
57. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C et al. (2012) EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 492: 108-112. doi:10.1038/nature11606. PubMed: 23051747.
58. Johnson KE, Wilgus TA (2012) Multiple roles for VEGF in nonmelanoma skin cancer: angiogenesis and beyond. J Skin Cancer 2012: 483439
59. Beck B, Driessens G, Goossens S, Youssef KK, Kuchnio A et al. (2011) A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478: 399-403. doi:10.1038/nature10525. PubMed: 22012397.
60. Bortolomai I, Canevari S, Facetti I, De CL, Castellano G et al. (2010) Tumor initiating cells: development and critical characterization of a model derived from the A431 carcinoma cell line forming spheres in suspension. Cell Cycle 9: 1194-1206. doi:10.4161/cc.9.6.11108. PubMed: 20237414.
61. Geng S, Guo Y, Wang Q, Li L, Wang J (2013) Cancer stem-like cells enriched with CD29 and CD44 markers exhibit molecular characteristics with epithelial-mesenchymal transition in squamous cell carcinoma. Arch Dermatol Res 305: 35-47. doi:10.1007/s00403-012-1260-2. PubMed: 22740085.
62. Geng S, Wang Q, Wang J, Hu Z, Liu C et al. (2011) Isolation and identification of a distinct side population cancer cells in the human epidermal squamous cancer cell line A431. Arch Dermatol Res 303: 181-189. doi:10.1007/s00403-010-1100-1. PubMed: 21240514.
63. Rheinwald JG, Beckett MA (1981) Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer Res 41: 1657-1663. PubMed: 7214336. (Pubitemid 11114553)
64. Streit M, Velasco P, Brown LF, Skobe M, Richard L et al. (1999) Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas. Am J Pathol 155: 441-452. doi:10.1016/S0002-9440(10)65140-1. PubMed: 10433937. (Pubitemid 29370394)