Cervical cancer stem cells selectively overexpress HPV oncoprotein E6 that controls stemness and self-renewal through upregulation of HES1

Clinical Cancer Research

Volumn 22, Issue 16, 2016, Pages 4170-4184

  Tyagi, Abhishek ^a,b,c   Vishnoi, Kanchan ^b   Mahata, Sutapa ^b   Verma, Gaurav ^b   Srivastava, Yogesh ^b   Masaldan, Shashank ^b   Roy, Bal Gangadhar ^d   Bharti, Alok C ^b,e   Das, Bhudev C ^a,c  

^a AMITY UNIVERSITY   (India)

^b Institute of Cytology and Preventive Oncology (ICMR)   (India)

^c UNIVERSITY OF DELHI   (India)

^d INSTITUTE OF NUCLEAR MEDICINE AND ALLIED SCIENCES   (India)

^e UNIVERSITY OF DELHI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CD71 ANTIGEN; CELL PROTEIN; LRIG1 PROTEIN; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN E6; SMALL INTERFERING RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; ABC TRANSPORTER; BIOLOGICAL MARKER; HES1 PROTEIN, HUMAN; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL RENEWAL; CERVICAL CANCER CELL LINE; CULTURE MEDIUM; ENRICHMENT CULTURE; EXPERIMENTAL STUDY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR SPHEROID; TUMOR XENOGRAFT; UPREGULATION; UTERINE CERVIX CANCER; WART VIRUS; ANIMAL; BIOLOGICAL MODEL; CELL SELF-RENEWAL; CELL TRANSFORMATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; METABOLISM; NONOBESE DIABETIC MOUSE; ONCOGENE; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; UTERINE CERVIX TUMOR; VIRUS CELL TRANSFORMATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOMARKERS; CELL LINE, TUMOR; CELL SELF RENEWAL; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSFORMATION, VIRAL; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, FOS; GENES, JUN; HELA CELLS; HUMANS; MICE; MICE, INBRED NOD; MODELS, BIOLOGICAL; NEOPLASTIC STEM CELLS; ONCOGENE PROTEINS, VIRAL; PROTEIN INTERACTION MAPS; RECEPTOR, NOTCH1; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES-1; UTERINE CERVICAL NEOPLASMS;

EID: 84982085567     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2574     Document Type: Article

References (52)

1. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002;2:342-50.
2. Das BC, Sehgal A, Murthy NS, Gopalkrishna V, Sharma JK, Das DK, et al. Human papillomavirus and cervical cancer in Indian women. Lancet 1989;2:1271.
3. Das BC, Hussain S, Nasare V, Bharadwaj M. Prospects and prejudices of human papillomavirus vaccines in India. Vaccine 2008;26:2669-79.
4. Pectasides D, Kamposioras K, Papaxoinis G, Pectasides E. Chemotherapy for recurrent cervical cancer. Cancer Treat Rev 2008;34:603-13.
5. Ho GY, Burk RD, Klein S, Kadish AS, Chang CJ, Palan P, et al. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst 1995;87:1365-71.
6. Wu W, Vieira J, Fiore N, Banerjee P, Sieburg M, Rochford R, et al. KSHV/HHV-8 infection of human hematopoietic progenitor (CD34+) cells: persistence of infection during hematopoiesis invitro and invivo. Blood 2006;108:141-51.
7. Martens JE, Arends J, Van der Linden PJ, De Boer BA, Helmerhorst TJ. Cytokeratin 17 and p63 are markers of the HPV target cell, the cervical stem cell. Anticancer Res 2004;24:771-5.
8. Herfs M, Yamamoto Y, Laury A, Wang X, Nucci MR, McLaughlin-Drubin ME, et al. A discrete population of squamocolumnar junction cells implicated in the pathogenesis of cervical cancer. Proc Natl Acad Sci U S A 2012;109:10516-21.
9. Feng D, Peng C, Li C, Zhou Y, Li M, Ling B, et al. Identification and characterization of cancer stem-like cells from primary carcinoma of the cervix uteri. Oncol Rep 2009;22:1129-34.
10. Lopez J, Poitevin A, Mendoza-Martinez V, Perez-Plasencia C, Garcia-Carranca A. Cancer-initiating cells derived from established cervical cell lines exhibit stem-cell markers and increased radioresistance. BMC Cancer 2012;12:48.
11. Dyson N, Howley PM, Munger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 1989;243:934-7.
12. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 1990;248:76-9.
13. Talora C, Cialfi S, Segatto O, Morrone S, Kim Choi J, Frati L, et al. Constitutively active Notch1 induces growth arrestof HPV-positive cervical cancer cells via separate signaling pathways. Exp Cell Res 2005;305:343-54.
14. Henken FE, De-Castro Arce J, Rosl F, Bosch L, Meijer CJ, Snijders PJ, et al. The functional role of Notch signaling in HPV-mediated transformation is dose-dependent and linked to AP-1 alterations. Cell Oncol 2012;35:77-84.
15. Chiba S. Notch signaling in stem cell systems. Stem Cells 2006;24:2437-47.
16. Jensen KB, Watt FM. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci U S A 2006;103:11958-63.
17. Turin I, Schiavo R, Maestri M, Luinetti O, Bello B, Paulli M, et al. In vitro efficient expansion of tumor cells deriving from different types of human tumor samples. Med Sci 2014;2:70-81.
18. Telford WG, Bradford J, Godfrey W, Robey RW, Bates SE. Side population analysis using a violet-excited cell-permeable DNA binding dye. Stem Cells 2007;25:1029-36.
19. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. Invitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003;17:1253-70.
20. Dey D, Saxena M, Paranjape AN, Krishnan V, Giraddi R, Kumar MV, et al. Phenotypic and functional characterization of human mammary stem/progenitor cells in long term culture. PLoS One 2009;4:e5329.
21. Shukla S, Mahata S, Shishodia G, Pande S, Verma G, Hedau S, et al. Physical state & copy number of high risk human papillomavirus type 16 DNA in progression of cervical cancer. Indian J Med Res 2014;139:531-43.
22. Shukla S, Shishodia G, Mahata S, Hedau S, Pandey A, Bhambhani S, et al. Aberrant expression and constitutive activation of STAT3 in cervical carcinogenesis: implications in high-risk human papillomavirus infection. Mol Cancer 2010;9:282.
23. Bharti AC, Donato N, Singh S, Aggarwal BB. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factorkappa B and IkappaBalpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis. Blood 2003;101:1053-62.
24. Katoh M. Integrative genomic analyses on HES/HEY family: Notch-independent HES1, HES3 transcription in undifferentiated ES cells, and Notchdependent HES1, HES5, HEY1, HEY2, HEYL transcription in fetal tissues, adult tissues, or cancer. Int J Oncol 2007;31:461-6.
25. Weiswald LB, Guinebretiere JM, Richon S, Bellet D, Saubamea B, Dangles-Marie V. Insitu protein expression in tumour spheres: development of an immunostaining protocol for confocal microscopy. BMC Cancer 2010;10:106.
26. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
27. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science 1977;197:461-3.
28. Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and invivo. Nat Protoc 2009;4:1798-806.
29. Shukla S, Mahata S, Shishodia G, Pandey A, Tyagi A, Vishnoi K, et al. Functional regulatory role of STAT3 in HPV16-mediated cervical carcinogenesis. PLoS One 2013;8:e67849.
30. Janzen DM, Cheng D, Schafenacker AM, Paik DY, Goldstein AS, Witte ON, et al. Estrogen and progesterone together expand murine endometrial epithelial progenitor cells. Stem Cells 2013;31:808-22.
31. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013;41:D808-15.
32. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996;183:1797-806.
33. Rabindran SK, Ross DD, Doyle LA, Yang W, Greenberger LM. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res 2000;60:47-50.
34. Villanueva-Toledo J, Ponciano-Gomez A, Ortiz-Sanchez E, Garrido E. Side populations from cervical-cancer-derived cell lines have stem-cell-like properties. Mol Biol Rep 2014;41:1993-2004.
35. Bruno L, Hoffmann R, McBlane F, Brown J, Gupta R, Joshi C, et al. Molecular signatures of self-renewal, differentiation, and lineage choice in multipotential hemopoietic progenitor cells invitro. Mol Cell Biol 2004;24:741-56.
36. Hufbauer M, Biddle A, Borgogna C, Gariglio M, Doorbar J, Storey A, et al. Expression of betapapillomavirus oncogenes increases the number of keratinocytes with stem cell-like properties. J Virol 2013;87:12158-65.
37. Li A, Pouliot N, Redvers R, Kaur P. Extensive tissue-regenerative capacity of neonatal human keratinocyte stem cells and their progeny. J Clin Invest 2004;113:390-400.
38. Patel SA, Ramkissoon SH, Bryan M, Pliner LF, Dontu G, Patel PS, et al. Delineation of breast cancer cell hierarchy identifies the subset responsible for dormancy. Sci Rep 2012;2:906.
39. Tan TM, Gloss B, Bernard HU, Ting RC. Mechanism of translation of the bicistronic mRNA encoding human papillomavirus type 16 E6-E7 genes. J Gen Virol 1994;75:2663-70.
40. Lee SH, Lee CR, Rigas NK, Kim RH, Kang MK, Park NH, et al. Human papillomavirus 16 (HPV16) enhances tumor growth and cancer stemness of HPV-negative oral/oropharyngeal squamous cell carcinoma cells via miR-181 regulation. Papillomavirus Res 2015;1:116-25.
41. Valcourt JR, Lemons JM, Haley EM, Kojima M, Demuren OO, Coller HA. Staying alive: metabolic adaptations to quiescence. Cell Cycle 2012;11:1680-96.
42. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-56.
43. Ji J, Zheng PS. Expression of Sox2 in human cervical carcinogenesis. Hum Pathol 2010;41:1438-47.
44. Wang Z, Li Y, Sarkar FH. Notch signaling proteins: legitimate targets for cancer therapy. Curr Protein Pept Sci 2010;11:398-408.
45. Weijzen S, Zlobin A, Braid M, Miele L, Kast WM. HPV16 E6 and E7 oncoproteins regulate Notch-1 expression and cooperate to induce transformation. J Cell Physiol 2003;194:356-62.
46. Bhattacharya S, Das A, Mallya K, Ahmad I. Maintenance of retinal stem cells by Abcg2 is regulated by notch signaling. J Cell Sci 2007;120:2652-62.
47. Zhou X, Smith AJ, Waterhouse A, Blin G, Malaguti M, Lin CY, et al. Hes1 desynchronizes differentiation of pluripotent cells by modulating STAT3 activity. Stem Cells 2013;31:1511-22.
48. Curry CL, Reed LL, Nickoloff BJ, Miele L, Foreman KE. Notch-independent regulation of Hes-1 expression by c-Jun. N-terminal kinase signaling in human endothelial cells. Lab Invest 2006;86:842-52.
49. Vliet-Gregg PA, Hamilton JR, Katzenellenbogen RA. Human papillomavirus 16E6 and NFX1-123 potentiate Notch signaling and differentiation without activating cellular arrest. Virology 2015;478:50-60.
50. Ren C, Cheng X, Lu B, Yang G. Activation of interleukin-6/signal transducer and activator of transcription 3 by human papillomavirus early proteins 6 induces fibroblast senescence to promote cervical tumourigenesis through autocrine and paracrine pathways in tumour microenvironment. Eur J Cancer 2013;49:3889-99.
51. Rosl F, Das BC, Lengert M, Geletneky K, zur Hausen H. Antioxidantinduced changes of the AP-1 transcription complex are paralleled by a selective suppression of human papillomavirus transcription. J Virol 1997;71:362-70.
52. Prusty BK, Das BC. Constitutive activation of transcription factor AP-1 in cervical cancer and suppression of human papillomavirus (HPV) transcription and AP-1 activity in HeLa cells by curcumin. Int J Cancer 2005;113:951-60.