Cervical cancer stem cells: opportunities and challenges

Journal of Cancer Research and Clinical Oncology

Volumn 141, Issue 11, 2015, Pages 1889-1897

  Chhabra, Ravindresh ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Cancer therapeutics; CD49f; CSC; SOX2

Indexed keywords

ANTINEOPLASTIC AGENT; BMI1 PROTEIN; KRUPPEL LIKE FACTOR 4; MICRORNA; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UTF1 PROTEIN; TUMOR MARKER;

CANCER STEM CELL; CANCER SURVIVAL; CANCER THERAPY; CELL RENEWAL; CERVICAL CANCER CELL LINE; FEMALE; HUMAN; MARKER GENE; PRIORITY JOURNAL; REVIEW; SURVIVAL RATE; UTERINE CERVIX CANCER; BIOSYNTHESIS; CELL TRANSFORMATION; DRUG RESISTANCE; GENE TARGETING; GENETICS; PATHOLOGY; TUMOR RECURRENCE; UTERINE CERVICAL NEOPLASMS;

BIOMARKERS, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE TARGETING; HUMANS; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; UTERINE CERVICAL NEOPLASMS;

EID: 84951567946     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1905-y     Document Type: Review

References (88)

1. Akunuru S, James Zhai Q, Zheng Y (2012) Non-small cell lung cancer stem/progenitor cells are enriched in multiple distinct phenotypic subpopulations and exhibit plasticity. Cell Death Dis 3:e352. doi:10.1038/cddis.2012.93
2. Al-Hajj M, Wicha MS, Benito-Hernandez A et al (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100:3983–3988
3. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3:730–737
4. Bortolomai I, Canevari S, Facetti I 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
5. Boyer LA, Lee TI, Cole MF et al (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947–956. doi:10.1016/j.cell.2005.08.020
6. Bracken AP, Dietrich N, Pasini D et al (2006) Genome-wide mapping of polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20:1123–1136. doi:10.1101/gad.381706
7. Campbell LL, Polyak K (2007) Breast tumor heterogeneity: cancer stem cells or clonal evolution? Cell Cycle 6:2332–2338. doi:10.4161/cc.6.19.4914
8. Castellsagué X, Muñoz N (2003) Chapter 3: Cofactors in human papillomavirus carcinogenesis–role of parity, oral contraceptives, and tobacco smoking. J Natl Cancer Inst Monogr 20–28
9. Chaudary N, Pintilie M, Hedley D et al (2012) Hedgehog pathway signaling in cervical carcinoma and outcome after chemoradiation. Cancer 118:3105–3115. doi:10.1002/cncr.26635
10. Cheng W, Liu T, Wan X et al (2012) MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. FEBS J 279:2047–2059. doi:10.1111/j.1742-4658.2012.08589.x
11. Chhabra R, Saini N (2014) microRNAs in cancer stem cells: current status and future directions. Tumour Biol 35:8395–8405. doi:10.1007/s13277-014-2264-7
12. Collins AT, Berry PA, Hyde C et al (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65:10946–10951. doi:10.1158/0008-5472.CAN-05-2018
13. Crum CP, McKeon FD (2010) p63 in epithelial survival, germ cell surveillance, and neoplasia. Annu Rev Pathol 5:349–371. doi:10.1146/annurev-pathol-121808-102117
14. Dalerba P, Cho RW, Clarke MF (2007a) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284. doi:10.1146/annurev.med.58.062105.204854
15. Dalerba P, Dylla SJ, Park I-K et al (2007b) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104:10158–10163
16. Dean M, Fojo T, Bates S (2005) Tumour stem cells and drug resistance. Nat Rev Cancer 5:275–284
17. Dontu G, Abdallah WM, Foley JM et al (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 17:1253–1270. doi:10.1101/gad.1061803
18. Endo K, Terada T (2000) Protein expression of CD44 (standard and variant isoforms) in hepatocellular carcinoma: relationships with tumor grade, clinicopathologic parameters, p53 expression, and patient survival. J Hepatol 32:78–84. doi:10.1016/S0168-8278(00)80192-0
19. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M PD, Forman D, Bray F (2013) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase. No. 11 [Internet]. Lyon, Fr Int Agency Res Cancer 11. http://globocan.iarc.f
20. Ginestier C, Hur MH, Charafe-Jauffret E 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
21. Golebiewska A, Brons NHC, Bjerkvig R, Niclou SP (2011) Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8:136–147
22. Govan VA (2008) A novel vaccine for cervical cancer: quadrivalent human papillomavirus (types 6, 11, 16 and 18) recombinant vaccine (Gardasil). Ther Clin Risk Manag 4:65–70
23. Gu W, Yeo E, McMillan N, Yu C (2011) Silencing oncogene expression in cervical cancer stem-like cells inhibits their cell growth and self-renewal ability. Cancer Gene Ther 18:897–905. doi:10.1038/cgt.2011.58
24. Guenin S, Mouallif M, Deplus R et al (2012) Aberrant promoter methylation and expression of UTF1 during cervical carcinogenesis. PLoS One. doi:10.1371/journal.pone.0042704
25. Gupta PB, Chaffer CL, Weinberg RA (2009) Cancer stem cells: mirage or reality? Nat Med 15:1010–1012. doi:10.1038/nm0909-1010
26. Gupta PB, Fillmore CM, Jiang G et al (2011) Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146:633–644. doi:10.1016/j.cell.2011.07.026
27. Hanahan D (2000) The Hallmarks of Cancer. Cell 100:57–70. doi:10.1016/S0092-8674(00)81683-9
28. Henry JC, Park J-K, Jiang J et al (2010) miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem Biophys Res Commun 403:120–125. doi:10.1016/j.bbrc.2010.10.130
29. Herfs M, Yamamoto Y, Laury A et al (2012) A discrete population of squamocolumnar junction cells implicated in the pathogenesis of cervical cancer. Proc Natl Acad Sci 109:10516–10521. doi:10.1073/pnas.1202684109
30. Higgins C (2012) Understanding laboratory investigations: A guide for nurses, midwives and health professionals, 3rd edn. Wiley-Blackwell, ISBN: 978-0-470-65951-9
31. Huang EH, Hynes MJ, Zhang T 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
32. Ji J, Zheng PS (2010) Expression of Sox2 in human cervical carcinogenesis. Hum Pathol 41:1438–1447. doi:10.1016/j.humpath.2009.11.021
33. Jordan CT (2009) Cancer stem cells: controversial or just misunderstood? Cell Stem Cell 4:203–205. doi:10.1016/j.stem.2009.02.003
34. Karjane N, Chelmow D (2013) New cervical cancer screening guidelines, again. Obstet Gynecol Clin N Am 40:211–223. doi:10.1016/j.ogc.2013.03.001
35. Kryczek I, Liu S, Roh M et al (2012) Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells. Int J Cancer 130:29–39. doi:10.1002/ijc.25967
36. Lalande ME, Miller RG (1979) Fluorescence flow analysis of lymphocyte activation using Hoechst 33342 dye. J Histochem Cytochem 27:394–397. doi:10.1177/27.1.86569
37. Landen CN, Goodman B, Katre AA et al (2010) Targeting aldehyde dehydrogenase cancer stem cells in ovarian cancer. Mol Cancer Ther 9:3186–3199. doi:10.1158/1535-7163.MCT-10-0563
38. Li L, Xie T (2005) Stem cell niche: structure and function. Annu Rev Cell Dev Biol 21:605–631. doi:10.1146/annurev.cellbio.21.012704.131525
39. Li C, Heidt DG, Dalerba P et al (2007) Identification of pancreatic cancer stem cells. Cancer Res 67:1030–1037. doi:10.1158/0008-5472.CAN-06-2030
40. Liu S, Zheng P (2013) High aldehyde dehydrogenase activity identifies cancer stem cells in human cervical cancer. Oncotarget 4(12):2462–2475
41. Liu X-F, Yang W-T, Xu R et al (2014) Cervical cancer cells with positive Sox2 expression exhibit the properties of cancer stem cells. PLoS One 9:e87092. doi:10.1371/journal.pone.0087092
42. Liu J, Cao X-C, Xiao Q, Quan M-F (2015) Apigenin inhibits HeLa sphere–forming cells through inactivation of casein kinase 2α. Mol Med Rep 11:665–669. doi:10.3892/mmr.2014.2720
43. Lobo NA, Shimono Y, Qian D, Clarke MF (2007) The biology of cancer stem cells. Annu Rev Cell Dev Biol 23:675–699. doi:10.1146/annurev.cellbio.22.010305.104154
44. López J, Poitevin A, Mendoza-Martínez V et al (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
45. Lu J-W, Chang J-G, Yeh K-T et al (2011) Overexpression of Thy1/CD90 in human hepatocellular carcinoma is associated with HBV infection and poor prognosis. Acta Histochem 113:833–838. doi:10.1016/j.acthis.2011.01.001
46. Maliekal TT, Bajaj J, Giri V et al (2008) The role of Notch signaling in human cervical cancer: implications for solid tumors. Oncogene 27:5110–5114. doi:10.1038/onc.2008.224
47. Meng E, Long B, Sullivan P et al (2012) CD44+/CD24− ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin Exp Metastasis. doi:10.1007/s10585-012-9482-4
48. Min L, Dong-Xiang S, Xiao-Tong G et al (2011) Clinicopathological and prognostic significance of Bmi-1 expression in human cervical cancer. Acta Obstet Gynecol Scand 90:737–745. doi:10.1111/j.1600-0412.2011.01102.x
49. 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
50. Organista-Nava J, Gómez-Gómez Y, Gariglio P (2014) Embryonic stem cell-specific signature in cervical cancer. Tumor Biol 35:1727–1738. doi:10.1007/s13277-013-1321-y
51. Pomfret TC, Gagnon JM, Gilchrist AT (2011) Quadrivalent human papillomavirus (HPV) vaccine: a review of safety, efficacy, and pharmacoeconomics. J Clin Pharm Ther 36:1–9. doi:10.1111/j.1365-2710.2009.01150.x
52. Qi W, Zhao C, Zhao L et al (2014) Sorting and identification of side population cells in the human cervical cancer cell line HeLa. Cancer Cell Int 14:3. doi:10.1186/1475-2867-14-3
53. Quade BJ, Yang A, Wang Y et al (2001) Expression of the p53 homologue p63 in early cervical neoplasia. Gynecol Oncol 80:24–29. doi:10.1006/gyno.2000.5953
54. Rao Q-X, Yao T-T, Zhang B-Z et al (2012) Expression and functional role of ALDH1 in cervical carcinoma cells. Asian Pac J Cancer Prev 13:1325–1331
55. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111. doi:10.1038/35102167
56. Rogers LJ, Eva LJ, Luesley DM (2008) Vaccines against cervical cancer. Curr Opin Oncol 20:570–574. doi:10.1517/14712598.4.11.1803
57. Samarzija I, Beard P (2012) Hedgehog pathway regulators influence cervical cancer cell proliferation, survival and migration. Biochem Biophys Res Commun 425:64–69. doi:10.1016/j.bbrc.2012.07.051
58. Sasaki A, Kamiyama T, Yokoo H et al (2010) Cytoplasmic expression of CD133 is an important risk factor for overall survival in hepatocellular carcinoma. Oncol Rep 24:537–546. doi:10.3892/or_00000890
59. Sell S (2010) On the stem cell origin of cancer. Am J Pathol 176:2584–2594. doi:10.2353/ajpath.2010.091064
60. Singh SK, Clarke ID, Terasaki M et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828. doi:10.1038/nature03128
61. Song B, Wang Y, Xi Y et al (2009) Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 28:4065–4074
62. Song B, Wang Y, Titmus MA et al (2010) Molecular mechanism of chemoresistance by miR-215 in osteosarcoma and colon cancer cells. Mol Cancer 9:96
63. Sullivan JP, Spinola M, Dodge M et al (2010) Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 70:9937–9948. doi:10.1158/0008-5472.CAN-10-0881
64. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. doi:10.1016/j.cell.2006.07.024
65. Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872. doi:10.1016/j.cell.2007.11.019
66. Takebe N, Ivy SP (2010) Controversies in cancer stem cells: targeting embryonic signaling pathways. Clin Cancer Res 16:3106–3112. doi:10.1158/1078-0432.CCR-09-2934
67. Thomas M, Narayan N, Pim D et al (2008) Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27:7018–7030. doi:10.1038/onc.2008.351
68. Tong YQ, Liu B, Zheng HY et al (2012) Overexpression of BMI-1 is associated with poor prognosis in cervical cancer. Asia Pac J Clin Oncol. doi:10.1111/j.1743-7563.2012.01564.x
69. Ucar D, Cogle CR, Zucali JR et al (2009) Aldehyde dehydrogenase activity as a functional marker for lung cancer. Chem Interact 178:48–55
70. Uren A, Fallen S, Yuan H et al (2005) Activation of the canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Cancer Res 65:6199–6206. doi:10.1158/0008-5472.CAN-05-0455
71. Van den Hoogen C, van der Horst G, Cheung H et al (2010) High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res 70:5163–5173. doi:10.1158/0008-5472.CAN-09-3806
72. Van Rhenen A, Feller N, Kelder A et al (2005) High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin Cancer Res 11:6520–6527. doi:10.1158/1078-0432.CCR-05-0468
73. Walboomers JM, Jacobs MV, Manos MM et al (1999) Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189:12–19. doi:10.1002/(SICI)1096-9896(199909)189:1<12:AID-PATH431>3.0.CO;2-F
74. Wang K, Zeng J, Luo L et al (2013a) Identification of a cancer stem cell-like side population in the HeLa human cervical carcinoma cell line. Oncol Lett 6:1673–1680. doi:10.3892/ol.2013.1607
75. Wang L, Guo H, Yang L et al (2013b) Morusin inhibits human cervical cancer stem cell growth and migration through attenuation of NF-κB activity and apoptosis induction. Mol Cell Biochem 379:7–18. doi:10.1007/s11010-013-1621-y
76. Wang P, Gao Q, Suo Z et al (2013c) Identification and characterization of cells with cancer stem cell properties in human primary lung cancer cell lines. PLoS One 8:e57020. doi:10.1371/journal.pone.0057020
77. Wang Y-D, Cai N, Wu X-L et al (2013d) OCT4 promotes tumorigenesis and inhibits apoptosis of cervical cancer cells by miR-125b/BAK1 pathway. Cell Death Dis 4:e760. doi:10.1038/cddis.2013.272
78. Wang D, Upadhyaya B, Liu Y et al (2014) Phenethyl isothiocyanate upregulates death receptors 4 and 5 and inhibits proliferation in human cancer stem-like cells. BMC Cancer 14:591. doi:10.1186/1471-2407-14-591
79. Wu XL, Zheng PS (2013) Undifferentiated embryonic cell transcription factor-1 (UTF1) inhibits the growth of cervical cancer cells by transactivating p27kip1. Carcinogenesis 34:1660–1668. doi:10.1093/carcin/bgt102
80. Yang WT, Zheng PS (2012) Kruppel-like factor 4 functions as a tumor suppressor in cervical carcinoma. Cancer 118:3691–3702. doi:10.1002/cncr.26698
81. Yang ZF, Ho DW, Ng MN et al (2008) Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13:153–166. doi:10.1016/j.ccr.2008.01.013
82. Yang Y, Wang Y, Yin C, Li X (2014a) Clinical significance of the stem cell gene Oct-4 in cervical cancer. Tumour Biol 35:5339–5345. doi:10.1007/s13277-014-1696-4
83. Yang Z, Pan X, Gao A, Zhu W (2014b) Expression of Sox2 in cervical squamous cell carcinoma. J BUON 19:203–206
84. Yao T, Chen Q, Zhang B et al (2011) The expression of ALDH1 in cervical carcinoma. Med Sci Monit 17:HY21–HY26
85. Zeppernick F, Ahmadi R, Campos B et al (2008) Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 14:123–129. doi:10.1158/1078-0432.CCR-07-0932
86. Zhang X, Wang C-X, Zhu C et al (2010) Overexpression of Bmi-1 in uterine cervical cancer: correlation with clinicopathology and prognosis. Int J Gynecol Cancer 20:1597–1603. doi:10.1111/IGC.0b013e3181fd080e
87. Zhang S-L, Wang Y-S, Zhou T et al (2012) Isolation and characterization of cancer stem cells from cervical cancer HeLa cells. Cytotechnology 64:477–484. doi:10.1007/s10616-012-9436-3
88. Zhu Z, Hao X, Yan M et al (2010) Cancer stem/progenitor cells are highly enriched in CD133+CD44+ population in hepatocellular carcinoma. Int J Cancer 126:2067–2078. doi:10.1002/ijc.24868