Stem cells in squamous head and neck cancer

Critical Reviews in Oncology/Hematology

Volumn 81, Issue 3, 2012, Pages 224-240

  Albers, Andreas E ^a   Chen, Chao ^a,b   Köberle, Beate ^c   Qian, Xu ^a   Klussmann, Jens P ^d   Wollenberg, Barbara ^e   Kaufmann, Andreas M ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b ZHEJIANG CANCER HOSPITAL   (China)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d UNIVERSITY HOSPITAL GIESSEN   (Germany)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

ALDH1; Chemoresistance; Epithelial mesenchymal transition; Human papillomavirus; Immunotherapy; Metastasis; Nanog; Oct3 4; Radioresistance; Sox2; Stemness

Indexed keywords

ALCOHOL ABUSE; CANCER STEM CELL; CHEMORADIOTHERAPY; DRUG TARGETING; EPITHELIAL STEM CELL; HEAD AND NECK CARCINOMA; HUMAN; IMMUNOGENICITY; METASTASIS; NONHUMAN; OUTCOME ASSESSMENT; PAPILLOMAVIRUS INFECTION; PHYSICAL SENSITIVITY; REVIEW; SQUAMOUS CELL CARCINOMA; STEM CELL; TOBACCO DEPENDENCE;

ALCOHOLISM; ALPHAPAPILLOMAVIRUS; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; MALE; NEOPLASM METASTASIS; NEOPLASMS, SQUAMOUS CELL; NEOPLASTIC STEM CELLS; PAPILLOMAVIRUS INFECTIONS; SMOKING; TIME FACTORS; TUMOR MARKERS, BIOLOGICAL;

EID: 84863034330     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2011.03.004     Document Type: Review

References (168)

1. Greenlee R.T., Hill-Harmon M.B., Murray T., Thun M. Cancer statistics, 2001. CA Cancer J Clin 2001, 51:15-36.
2. Jones A.S., Morar P., Phillips D.E., Field J.K., Husband D., Helliwell T.R. Second primary tumors in patients with head and neck squamous cell carcinoma. Cancer 1995, 75:1343-1353.
3. Leemans C.R., Tiwari R., Nauta J.J., van der Waal I., Snow G.B. Recurrence at the primary site in head and neck cancer and the significance of neck lymph node metastases as a prognostic factor. Cancer 1994, 73:187-190.
4. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008, 8:755-768.
5. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
6. Gillison M.L., Shah K.V. Human papillomavirus-associated head and neck squamous cell carcinoma: mounting evidence for an etiologic role for human papillomavirus in a subset of head and neck cancers. Curr Opin Oncol 2001, 13:183-188.
7. Gillison M.L., Koch W.M., Capone R.B., et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000, 92:709-720.
8. Smith E.M., Summersgill K.F., Allen J., et al. Human papillomavirus and risk of laryngeal cancer. Ann Otol Rhinol Laryngol 2000, 109:1069-1076.
9. Torrente MC, Rodrigo JP, Haigentz Jr M, et al. Human papillomavirus infections in laryngeal cancer. Head Neck 2011;33:581-6.
10. Blomberg M, Nielsen A, Munk C, Kjaer SK. Trends in head and neck cancer incidence in Denmark, 1978-2007 - focus on human papillomavirus associated sites. Int J Cancer 2010.
11. Ryerson A.B., Peters E.S., Coughlin S.S., et al. Burden of potentially human papillomavirus-associated cancers of the oropharynx and oral cavity in the US, 1998-2003. Cancer 2008, 113:2901-2909.
12. Auluck A, Hislop G, Bajdik C, Poh C, Zhang L, Rosin M. Trends in oropharyngeal and oral cavity cancer incidence of human papillomavirus (HPV)-related and HPV-unrelated sites in a multicultural population: the British Columbia experience. Cancer 2010;116:2635-44.
13. Settle K., Posner M.R., Schumaker L.M., et al. Racial survival disparity in head and neck cancer results from low prevalence of human papillomavirus infection in black oropharyngeal cancer patients. Cancer Prev Res (Phila) 2009, 2:776-781.
14. Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24-35.
15. Martens J.E., Arends J., Van der Linden P.J., De Boer B.A., Helmerhorst T.J. Cytokeratin 17 and p63 are markers of the HPV target cell, the cervical stem cell. Anticancer Res 2004, 24:771-775.
16. Zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002, 2:342-350.
17. Anzenbacher P., Anzenbacherova E. Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci 2001, 58:737-747.
18. Hecht S.S. DNA adduct formation from tobacco-specific N-nitrosamines. Mutat Res 1999, 424:127-142.
19. Nair U., Bartsch H. Metabolic polymorphisms as susceptibility markers for lung and oral cavity cancer. IARC Sci Publ 2001, 154:271-290.
20. Uematsu F., Kikuchi H., Motomiya M., et al. Association between restriction fragment length polymorphism of the human cytochrome P450IIE1 gene and susceptibility to lung cancer. Jpn J Cancer Res 1991, 82:254-256.
21. Bensaad K., Vousden K.H. p53: new roles in metabolism. Trends Cell Biol 2007, 17:286-291.
22. Peltonen JK, Helppi HM, Paakko P, Turpeenniemi-Hujanen T, Vahakangas KH. p53 in head and neck cancer: functional consequences and environmental implications of TP53 mutations. Head Neck Oncol 2010;2:36.
23. Siemiatycki J., Richardson L., Straif K., et al. Listing occupational carcinogens. Environ Health Perspect 2004, 112:1447-1459.
24. Dai M., Clifford G.M., le Calvez F., et al. Human papillomavirus type 16 and TP53 mutation in oral cancer: matched analysis of the IARC multicenter study. Cancer Res 2004, 64:468-471.
25. Magnusson P.K., Sparen P., Gyllensten U.B. Genetic link to cervical tumours. Nature 1999, 400:29-30.
26. Parker A.C., Mundada L.V., Schmaier A.H., Fay W.P. Factor VLeiden inhibits fibrinolysis in vivo. Circulation 2004, 110:3594-3598.
27. Spardy N., Duensing A., Charles D., et al. The human papillomavirus type 16 E7 oncoprotein activates the Fanconi anemia (FA) pathway and causes accelerated chromosomal instability in FA cells. J Virol 2007, 81:13265-13270.
28. Albers A.E., Strauss L., Liao T., Hoffmann T.K., Kaufmann A.M. T cell-tumor interaction directs the development of immunotherapies in head and neck cancer. Clin Dev Immunol 2010, 236378.
29. Bau DT, Chang CH, Tsai MH, et al. Association between DNA repair gene ATM polymorphisms and oral cancer susceptibility. Laryngoscope 2010;12:2417-22.
30. Gal T.J., Huang W.Y., Chen C., Hayes R.B., Schwartz S.M. DNA repair gene polymorphisms and risk of second primary neoplasms and mortality in oral cancer patients. Laryngoscope 2005, 115:2221-2231.
31. Singh M., Shah P.P., Singh A.P., et al. Association of genetic polymorphisms in glutathione S-transferases and susceptibility to head and neck cancer. Mutat Res 2008, 638:184-194.
32. Lacko M., Oude Ophuis M.B., Peters W.H., Manni J.J. Genetic polymorphisms of smoking-related carcinogen detoxifying enzymes and head and neck cancer susceptibility. Anticancer Res 2009, 29:753-761.
33. Sliwinski T, Walczak A, Przybylowska K, et al. Polymorphisms of the XRCC3 C722T and the RAD51 G135C genes and the risk of head and neck cancer in a Polish population. Exp Mol Pathol 2010;89:358-66.
34. Singh A.P., Shah P.P., Ruwali M., Mathur N., Pant M.C., Parmar D. Polymorphism in cytochrome P4501A1 is significantly associated with head and neck cancer risk. Cancer Invest 2009, 27:869-876.
35. Sabitha K, Reddy MV, Jamil K. Smoking related risk involved in individuals carrying genetic variants of CYP1A1 gene in head and neck cancer. Cancer Epidemiol 2010;34:587-92.
36. Song N., Tan W., Xing D., Lin D. CYP 1A1 polymorphism and risk of lung cancer in relation to tobacco smoking: a case-control study in China. Carcinogenesis 2001, 22:11-16.
37. Bartsch H., Nair U., Risch A., Rojas M., Wikman H., Alexandrov K. Genetic polymorphism of CYP genes, alone or in combination, as a risk modifier of tobacco-related cancers. Cancer Epidemiol Biomarkers Prev 2000, 9:3-28.
38. Thier R., Bruning T., Roos P.H., et al. Markers of genetic susceptibility in human environmental hygiene and toxicology: the role of selected CYP, NAT and GST genes. Int J Hyg Environ Health 2003, 206:149-171.
39. Tanaka F, Yamamoto K, Suzuki S, et al. Strong interaction between the effects of alcohol consumption and smoking on oesophageal squamous cell carcinoma among individuals with ADH1B and/or ALDH2 risk alleles. Gut 2010;59:1457-64.
40. Wang J, Lippman SM, Lee JJ, et al. Genetic variations in regulator of G-protein signaling genes as susceptibility loci for second primary tumor/recurrence in head and neck squamous cell carcinoma. Carcinogenesis 2010;31:1755-61.
41. Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: models and concepts. Annu Rev Med 2007, 58:267-284.
42. Kennedy J.A., Barabe F., Poeppl A.G., Wang J.C., Dick J.E. Comment on "Tumor growth need not be driven by rare cancer stem cells". Science 2007, 318. 1722 author reply 1722.
43. Ginestier C., Hur M.H., Charafe-Jauffret E., et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567.
44. Dick J.E. Stem cell concepts renew cancer research. Blood 2008, 112:4793-4807.
45. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
46. Lapidot T., Sirard C., Vormoor J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
47. Schatton T., Frank N.Y., Frank M.H. Identification and targeting of cancer stem cells. Bioessays 2009, 31:1038-1049.
48. Fidler I.J., Hart I.R. Biological diversity in metastatic neoplasms: origins and implications. Science 1982, 217:998-1003.
49. Harper L.J., Piper K., Common J., Fortune F., Mackenzie I.C. Stem cell patterns in cell lines derived from head and neck squamous cell carcinoma. J Oral Pathol Med 2007, 36:594-603.
50. Hamburger A.W., Salmon S.E. Primary bioassay of human tumor stem cells. Science 1977, 197:461-463.
51. Sabbath K.D., Ball E.D., Larcom P., Davis R.B., Griffin J.D. Heterogeneity of clonogenic cells in acute myeloblastic leukemia. J Clin Invest 1985, 75:746-753.
52. Griffin J.D., Lowenberg B. Clonogenic cells in acute myeloblastic leukemia. Blood 1986, 68:1185-1195.
53. Lobo N.A., Shimono Y., Qian D., Clarke M.F. The biology of cancer stem cells. Annu Rev Cell Dev Biol 2007, 23:675-699.
54. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
55. Cortes-Dericks L., Carboni G.L., Schmid R.A., Karoubi G. Putative cancer stem cells in malignant pleural mesothelioma show resistance to cisplatin and pemetrexed. Int J Oncol 2010, 37:437-444.
56. Regenbrecht C.R., Lehrach H., Adjaye J. Stemming cancer: functional genomics of cancer stem cells in solid tumors. Stem Cell Rev 2008, 4:319-328.
57. Schiller JT, Day PM, Kines RC. Current understanding of the mechanism of HPV infection. Gynecol Oncol 2004;118:S12-7.
58. Fidler I.J., Kripke M.L. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977, 197:893-895.
59. Braakhuis B.J., Leemans C.R., Brakenhoff R.H. Expanding fields of genetically altered cells in head and neck squamous carcinogenesis. Semin Cancer Biol 2005, 15:113-120.
60. Desai P.C., Jaglal M.V., Gopal P., et al. Human papillomavirus in metastatic squamous carcinoma from unknown primaries in the head and neck: a retrospective 7 year study. Exp Mol Pathol 2009, 87:94-98.
61. Johnson K.M., Kines R.C., Roberts J.N., Lowy D.R., Schiller J.T., Day P.M. Role of heparan sulfate in attachment to and infection of the murine female genital tract by human papillomavirus. J Virol 2009, 83:2067-2074.
62. Pyeon D., Pearce S.M., Lank S.M., Ahlquist P., Lambert P.F. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 2009, 5:e1000318.
63. Vinokurova S., Wentzensen N., Einenkel J., et al. Clonal history of papillomavirus-induced dysplasia in the female lower genital tract. J Natl Cancer Inst 2005, 97:1816-1821.
64. Mani S.A., Guo W., Liao M.J., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
65. Morel A.P., Lievre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 2008, 3:e2888.
66. Turley E.A., Veiseh M., Radisky D.C., Bissell M.J. Mechanisms of disease: epithelial-mesenchymal transition--does cellular plasticity fuel neoplastic progression?. Nat Clin Pract Oncol 2008, 5:280-290.
67. Baum B., Settleman J., Quinlan M.P. Transitions between epithelial and mesenchymal states in development and disease. Semin Cell Dev Biol 2008, 19:294-308.
68. Lysy P.A., Smets F., Sibille C., Najimi M., Sokal E.M. Human skin fibroblasts: from mesodermal to hepatocyte-like differentiation. Hepatology 2007, 46:1574-1585.
69. Radisky D.C., LaBarge M.A. Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell 2008, 2:511-512.
70. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2:442-454.
71. Hermann P.C., Huber S.L., Herrler T., et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
72. Tsuji T., Ibaragi S., Shima K., et al. Epithelial-mesenchymal transition induced by growth suppressor p12CDK2-AP1 promotes tumor cell local invasion but suppresses distant colony growth. Cancer Res 2008, 68:10377-10386.
73. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat (Basel) 1995, 154:8-20.
74. Perez-Pomares J.M., Munoz-Chapuli R. Epithelial-mesenchymal transitions: a mesodermal cell strategy for evolutive innovation in Metazoans. Anat Rec 2002, 268:343-351.
75. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 2003, 15:740-746.
76. Savagner P., Kusewitt D.F., Carver E.A., et al. Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. J Cell Physiol 2005, 202:858-866.
77. Thomson S., Buck E., Petti F., et al. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res 2005, 65:9455-9462.
78. Frederick B.A., Helfrich B.A., Coldren C.D., et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther 2007, 6:1683-1691.
79. Black P.C., Brown G.A., Inamoto T., et al. Sensitivity to epidermal growth factor receptor inhibitor requires E-cadherin expression in urothelial carcinoma cells. Clin Cancer Res 2008, 14:1478-1486.
80. Hoshino H., Miyoshi N., Nagai K., et al. Epithelial-mesenchymal transition with expression of SNAI1-induced chemoresistance in colorectal cancer. Biochem Biophys Res Commun 2009, 390:1061-1065.
81. Kurrey N.K., Jalgaonkar S.P., Joglekar A.V., et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009, 27:2059-2068.
82. Wang Z., Li Y., Kong D., et al. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 2009, 69:2400-2407.
83. Kong D., Li Y., Wang Z., et al. miR-200 regulates PDGF-D-mediated epithelial-mesenchymal transition, adhesion, and invasion of prostate cancer cells. Stem Cells 2009, 27:1712-1721.
84. Chen C., Wei Y., Hummel M., et al. Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLoS ONE 2011, 6:e16466.
85. Kupferman ME, Jiffar T, El-Naggar A, et al. TrkB induces EMT and has a key role in invasion of head and neck squamous cell carcinoma. Oncogene 2010;29:2047-59.
86. Rampias T, Boutati E, Pectasides E, et al. Activation of Wnt signaling pathway by human papillomavirus E6 and E7 oncogenes in HPV16-positive oropharyngeal squamous carcinoma cells. Mol Cancer Res 2010;8:433-43.
87. Gupta P.B., Onder T.T., Jiang G., et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009, 138:645-659.
88. Pardal R., Clarke M.F., Morrison S.J. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 2003, 3:895-902.
89. Ma S., Chan K.W., Lee T.K., et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 2008, 6:1146-1153.
90. Jiang F., Qiu Q., Khanna A., et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009, 7:330-338.
91. Huang E.H., Hynes M.J., Zhang T., et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009, 69:3382-3389.
92. Chen Y.C., Chen Y.W., Hsu H.S., et al. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 2009, 385:307-313.
93. Prince M.E., Ailles L.E. Cancer stem cells in head and neck squamous cell cancer. J Clin Oncol 2008, 26:2871-2875.
94. Mack B., Gires O. CD44s and CD44v6 expression in head and neck epithelia. PLoS ONE 2008, 3:e3360.
95. Prince M.E., Sivanandan R., Kaczorowski A., et al. 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.
96. Douville J., Beaulieu R., Balicki D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cells Dev 2009, 18:17-25.
97. Jaksch M., Munera J., Bajpai R., Terskikh A., Oshima R.G. Cell cycle-dependent variation of a CD133 epitope in human embryonic stem cell, colon cancer, and melanoma cell lines. Cancer Res 2008, 68:7882-7886.
98. Chiou S.H., Yu C.C., Huang C.Y., et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res 2008, 14:4085-4095.
99. Singh S.K., Hawkins C., Clarke I.D., et al. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
100. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
101. Eramo A., Lotti F., Sette G., et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008, 15:504-514.
102. Wei X.D., Zhou L., Cheng L., Tian J., Jiang J.J., Maccallum J. In vivo investigation of CD133 as a putative marker of cancer stem cells in Hep-2 cell line. Head Neck 2009, 31:94-101.
103. Chen YC, Chang CJ, Hsu HS, et al. Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral Oncol 2009;46:158-65.
104. St John M.A., Dohadwala M., Luo J., et al. Proinflammatory mediators upregulate snail in head and neck squamous cell carcinoma. Clin Cancer Res 2009, 15:6018-6027.
105. Yang J., Mani S.A., Weinberg R.A. Exploring a new twist on tumor metastasis. Cancer Res 2006, 66:4549-4552.
106. Vered M, Dayan D, Yahalom R, et al. Cancer-associated fibroblasts and epithelial-mesenchymal transition in metastatic oral tongue squamous cell carcinoma. Int J Cancer 2010;127:1356-62.
107. Kashyap V., Rezende N.C., Scotland K.B., et al. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 2009, 18:1093-1108.
108. Rodda D.J., Chew J.L., Lim L.H., et al. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005, 280:24731-24737.
109. Pang R., Law W.L., Chu A.C., et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010, 6:603-615.
110. Clement V., Marino D., Cudalbu C., et al. Marker-independent identification of glioma-initiating cells. Nat Methods 2010, 7:224-228.
111. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988.
112. Hermann P.C., Huber S.L., Heeschen C. Metastatic cancer stem cells: a new target for anti-cancer therapy?. Cell Cycle 2008, 7:188-193.
113. Magni M., Shammah S., Schiro R., Mellado W., Dalla-Favera R., Gianni A.M. Induction of cyclophosphamide-resistance by aldehyde-dehydrogenase gene transfer. Blood 1996, 87:1097-1103.
114. Bozec A., Gros F.X., Penault-Llorca F., et al. Vertical VEGF targeting: A combination of ligand blockade with receptor tyrosine kinase inhibition. Eur J Cancer 2008, 44:1922-1930.
115. Bao S., Wu Q., McLendon R.E., et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
116. Li X., Lewis M.T., Huang J., et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679.
117. de Grouw E.P., Raaijmakers M.H., Boezeman J.B., et al. Preferential expression of a high number of ATP binding cassette transporters in both normal and leukemic CD34+CD38-cells. Leukemia 2006, 20:750-754.
118. Wulf G.G., Wang R.Y., Kuehnle I., et al. A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia. Blood 2001, 98:1166-1173.
119. Costello R.T., Mallet F., Gaugler B., et al. Human acute myeloid leukemia CD34+/CD38-progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res 2000, 60:4403-4411.
120. Liu G., Yuan X., Zeng Z., et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67.
121. Eramo A., Ricci-Vitiani L., Zeuner A., et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 2006, 13:1238-1241.
122. Phillips T.M., McBride W.H., Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006, 98:1777-1785.
123. Ma S., Lee T.K., Zheng B.J., Chan K.W., Guan X.Y. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008, 27:1749-1758.
124. Todaro M., Alea M.P., Di Stefano A.B., et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1:389-402.
125. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 1979, 59:527-605.
126. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat Rev Drug Discov 2009, 8:579-591.
127. Toyokuni S., Okamoto K., Yodoi J., Hiai H. Persistent oxidative stress in cancer. FEBS Lett 1995, 358:1-3.
128. Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 2010;48:749-62.
129. Park J.S., Sharma L.K., Li H., et al. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet 2009, 18:1578-1589.
130. Cerutti P.A. Prooxidant states and tumor promotion. Science 1985, 227:375-381.
131. Behrend L., Henderson G., Zwacka R.M. Reactive oxygen species in oncogenic transformation. Biochem Soc Trans 2003, 31:1441-1444.
132. Wu W.S. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev 2006, 25:695-705.
133. Mercurio F., Manning A.M. NF-kappaB as a primary regulator of the stress response. Oncogene 1999, 18:6163-6171.
134. Adler V., Yin Z., Fuchs S.Y., et al. Regulation of JNK signaling by GSTp. EMBO J 1999, 18:1321-1334.
135. Sundaresan M., Yu Z.X., Ferrans V.J., Irani K., Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299.
136. Guyton K.Z., Liu Y., Gorospe M., Xu Q., Holbrook N.J. Activation of mitogen-activated protein kinase by H2O2. Role in cell survival following oxidant injury. J Biol Chem 1996, 271:4138-4142.
137. Rao G.N. Hydrogen peroxide induces complex formation of SHC-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signal-regulated protein kinases group of mitogen-activated protein kinases. Oncogene 1996, 13:713-719.
138. Preston T.J., Abadi A., Wilson L., Singh G. Mitochondrial contributions to cancer cell physiology: potential for drug development. Adv Drug Deliv Rev 2001, 49:45-61.
139. Sun W., Zhou S., Chang S.S., McFate T., Verma A., Califano J.A. Mitochondrial mutations contribute to HIF1alpha accumulation via increased reactive oxygen species and up-regulated pyruvate dehydrogenease kinase 2 in head and neck squamous cell carcinoma. Clin Cancer Res 2009, 15:476-484.
140. Kim H.J., Chakravarti N., Oridate N., Choe C., Claret F.X., Lotan R. N-(4-hydroxyphenyl)retinamide-induced apoptosis triggered by reactive oxygen species is mediated by activation of MAPKs in head and neck squamous carcinoma cells. Oncogene 2006, 25:2785-2794.
141. Simons A.L., Parsons A.D., Foster K.A., Orcutt K.P., Fath M.A., Spitz D.R. Inhibition of glutathione and thioredoxin metabolism enhances sensitivity to perifosine in head and neck cancer cells. J Oncol 2009, 2009:519563.
142. Fribley A., Zeng Q., Wang C.Y. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol 2004, 24:9695-9704.
143. Kim J.S., Lee J.H., Jeong W.W., et al. Reactive oxygen species-dependent EndoG release mediates cisplatin-induced caspase-independent apoptosis in human head and neck squamous carcinoma cells. Int J Cancer 2008, 122:672-680.
144. Baumann M., Krause M., Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008, 8:545-554.
145. Jang Y.Y., Sharkis S.J. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007, 110:3056-3063.
146. Ito K., Hirao A., Arai F., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004, 431:997-1002.
147. Keith B., Simon M.C. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007, 129:465-472.
148. Simon M.C., Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 2008, 9:285-296.
149. Diehn M., Cho R.W., Lobo N.A., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
150. Tothova Z., Kollipara R., Huntly B.J., et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007, 128:325-339.
151. Visus C., Ito D., Amoscato A., et al. Identification of human aldehyde dehydrogenase 1 family member A1 as a novel CD8+ T-cell-defined tumor antigen in squamous cell carcinoma of the head and neck. Cancer Res 2007, 67:10538-10545.
152. Xu Q., Liu G., Yuan X., et al. Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens. Stem Cells 2009, 27:1734-1740.
153. Vlashi E., Kim K., Lagadec C., et al. In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 2009, 101:350-359.
154. Mellodew K., Suhr R., Uwanogho D.A., et al. Nestin expression is lost in a neural stem cell line through a mechanism involving the proteasome and Notch signalling. Brain Res Dev Brain Res 2004, 151:13-23.
155. Ben-Saadon R., Zaaroor D., Ziv T., Ciechanover A. The polycomb protein Ring1B generates self atypical mixed ubiquitin chains required for its in vitro histone H2A ligase activity. Mol Cell 2006, 24:701-711.
156. Schatton T., Murphy G.F., Frank N.Y., et al. Identification of cells initiating human melanomas. Nature 2008, 451:345-349.
157. Park C.Y., Tseng D., Weissman I.L. Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol Ther 2009, 17:219-230.
158. Chen J.S., Pardo F.S., Wang-Rodriguez J., et al. EGFR regulates the side population in head and neck squamous cell carcinoma. Laryngoscope 2006, 116:401-406.
159. Borjesson P.K., Postema E.J., Roos J.C., et al. Phase I therapy study with (186)Re-labeled humanized monoclonal antibody BIWA 4 (bivatuzumab) in patients with head and neck squamous cell carcinoma. Clin Cancer Res 2003, 9:3961S-3972S.
160. Colnot D.R., Quak J.J., Roos J.C., et al. Phase I therapy study of 186Re-labeled chimeric monoclonal antibody U36 in patients with squamous cell carcinoma of the head and neck. J Nucl Med 2000, 41:1999-2010.
161. Colnot D.R., Ossenkoppele G.J., Roos J.C., et al. Reinfusion of unprocessed, granulocyte colony-stimulating factor-stimulated whole blood allows dose escalation of 186Relabeled chimeric monoclonal antibody U36 radioimmunotherapy in a phase I dose escalation study. Clin Cancer Res 2002, 8:3401-3406.
162. Riechelmann H., Sauter A., Golze W., et al. Phase I trial with the CD44v6-targeting immunoconjugate bivatuzumab mertansine in head and neck squamous cell carcinoma. Oral Oncol 2008, 44:823-829.
163. Tijink B.M., Buter J., de Bree R., et al. A phase I dose escalation study with anti-CD44v6 bivatuzumab mertansine in patients with incurable squamous cell carcinoma of the head and neck or esophagus. Clin Cancer Res 2006, 12:6064-6072.
164. Barrallo-Gimeno A., Nieto M.A. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005, 132:3151-3161.
165. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006, 7:131-142.
166. Smith L.M., Nesterova A., Ryan M.C., et al. CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 2008, 99:100-109.
167. Jin L., Lee E.M., Ramshaw H.S., et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009, 5:31-42.
168. Piccirillo S.G., Reynolds B.A., Zanetti N., et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006, 444:761-765.