DOI QR코드

DOI QR Code

Cancer Stem Cells in Head and Neck Squamous Cell Carcinoma: A Review

  • Satpute, Pranali Shirish (Department of Oral and Maxillofacial Pathology, Government Dental College and Hospital) ;
  • Hazarey, Vinay (Department of Oral and Maxillofacial Pathology, Government Dental College and Hospital) ;
  • Ahmed, Riyaz (Department of Dentistry, Government Medical College and Hospital) ;
  • Yadav, Lalita (Department of Oral and Maxillofacial Pathology, Kalka Dental College and Hospital)
  • Published : 2013.10.30

Abstract

Research indicates that a small population of cancer cells is highly tumorigenic, endowed with the capacity for self-renewal, and has the ability to differentiate into cells that constitute the bulk of tumors. These cells are considered the "drivers" of the tumorigenic process in some tumor types, and have been named cancer stem cells (CSC). Epithelial-mesenchymal transition (EMT) appears to be involved in the process leading to the acquisition of stemness by epithelial tumor cells. Through this process, cells acquire an invasive phenotype that may contribute to tumor recurrence and metastasis. CSC have been identified in human head and neck squamous cell carcinomas (HNSCC) using markers such as CD133 and CD44 expression, and aldehyde dehydrogenase (ALDH) activity. Head and neck cancer stem cells reside primarily in perivascular niches in the invasive fronts where endothelial-cell initiated events contribute to their survival and function. Clinically, CSC enrichment has been shown to be enhanced in recurrent disease, treatment failure and metastasis. CSC represent a novel target of study given their slow growth and innate mechanisms conferring treatment resistance. Further understanding of their unique phenotype may reveal potential molecular targets to improve therapeutic and survival outcomes in patients with HNSCC. Here, we discuss the state-of-the-knowledge on the pathobiology of cancer stem cells, with a focus on the impact of these cells on head and neck tumor progression, metastasis and recurrence due to treatment failure.

Keywords

References

  1. Al-Hajj M, Wicha M, Benito-Hernandez A, et al (2003). Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA, 100, 3983-8. https://doi.org/10.1073/pnas.0530291100
  2. Allegra E, Garozzo A, Lombardo N, et al (2006). Mutations and polymorphisms in mitochondrial DNA in head and neck cancer cell lines. Acta Otorhinolaryngol Ital, 26, 185-90.
  3. Allegra E, Baudi F, La Boria A, et al (2009). Multiple head and neck tumours and their genetic relationship. Acta Otorhinolaryngol Ital, 29, 237-41.
  4. Allegra E, Trapasso S (2012). Cancer stem cells in head and neck cancer. Onco Targets and Therapy, 5, 375-83.
  5. Batlle E, Sancho E, Franci C, et al (2000). The transcription factor snail is a repressor of E-cadherin gene expression in the epithelial tumour cells. Nat Cell Biol, 2, 84-9. https://doi.org/10.1038/35000034
  6. Baumann M, Krause M (2010). CD44: a cancer stem cell-related biomarker with predictive potential for radiotherapy. Clin Cancer Res, 16, 5091-3. https://doi.org/10.1158/1078-0432.CCR-10-2244
  7. Bonnet D, Dick J (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med, 3, 730-7. https://doi.org/10.1038/nm0797-730
  8. Borovski T, De Souza E, Melo F, et al (2011). Cancer stem cell niche: the place to be. Cancer Res, 71, 634-9. https://doi.org/10.1158/0008-5472.CAN-10-3220
  9. Bosron W, Lumeng L, Li T (1988). Genetic polymorphism of enzymes of alcohol metabolism and susceptibility to alcoholic liver disease. Mol Aspects Med, 10, 147-58. https://doi.org/10.1016/0098-2997(88)90019-2
  10. Braakhuis B, Tabor M, Leemans C, et al (2002). Second primary tumors and field cancerization in oral and oropharyngeal cancer: molecular techniques provide new insights and definitions. Head Neck, 24, 198-206. https://doi.org/10.1002/hed.10042
  11. Braakhuis B, Leemans C, Brakenhoff RH, et al (2005). Expanding fields of genetically altered cells in head and neck squamous carcinogenesis. Semin Cancer Biol, 15, 113-20. https://doi.org/10.1016/j.semcancer.2004.08.004
  12. Califano J, Westra W, Meininger G, et al (2000). Genetic progression and clonal relationship of recurrent premalignant head and neck lesions. Clin Cancer Res, 2, 347-52.
  13. Cano A, Perez-Moreno M, Rodrigo I, et al (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol, 2, 76-83. https://doi.org/10.1038/35000025
  14. Carvalho A, Nishimoto I, Califano J, et al (2005). Trends in incidence and prognosis for head and neck cancer in the United States: a site-specific analysis of the SEER database. Int J Cancer, 114, 806-16. https://doi.org/10.1002/ijc.20740
  15. Chen C, Wei Y ,Hummel M, et al (2011). Evidence for epithelial- mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLoS One, 6, 16466. https://doi.org/10.1371/journal.pone.0016466
  16. Chen Y, Chen Y, Hsu H, 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, 307-13. https://doi.org/10.1016/j.bbrc.2009.05.048
  17. Cheng G, Chan J, Wang Q, et al (2007). Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion and resistance to paclitaxel. Cancer Res, 67, 1979-87. https://doi.org/10.1158/0008-5472.CAN-06-1479
  18. Chikamatsu K, Ishii H, Takahashi G, et al (2012). Resistance to apoptosis-inducing stimuli in CD44+ head and neck squamous cell carcinoma cells. Head Neck, 34, 336-43. https://doi.org/10.1002/hed.21732
  19. Chiou S, Yu C, Huang Y, et al (2008). Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high grade oral squamous cell carcinoma. Clin Cancer Res, 14, 4085-95. https://doi.org/10.1158/1078-0432.CCR-07-4404
  20. Clarke M, Dick J, Dirks P, et al (2006). Cancer stem cells: Perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res, 66, 9339-44. https://doi.org/10.1158/0008-5472.CAN-06-3126
  21. Cohnheim J (1875). Congenitales, quergestreiftes muskelsarkon der nireren. Virchows Arch, 65, 64. https://doi.org/10.1007/BF01978936
  22. Collins A, Berry P, Hyde C, et al (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res, 65, 10946-51. https://doi.org/10.1158/0008-5472.CAN-05-2018
  23. Dalerba P, Dylla S, Park I, et al (2007). Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA, 104, 10158-63. https://doi.org/10.1073/pnas.0703478104
  24. Davis S, Divi V, Owen J, et al (2010). Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma. arch otolaryngol. Head Neck Surg, 136, 1260-6. https://doi.org/10.1001/archoto.2010.219
  25. Durante F (1874). Nessus pathophysiological between the flaw structure of the mother and the genesis of some malignant tumors. Arch Memor Observ Chir Prat, 111, 217.
  26. Eramo A, Lotti F, Sette G, et al (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ, 15, 504-14. https://doi.org/10.1038/sj.cdd.4402283
  27. Fang D, Nguyen T, Leishear K, et al (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res, 65, 9328-37. https://doi.org/10.1158/0008-5472.CAN-05-1343
  28. Fuchs E, Tumbar T, Guasch G (2004). Socializing with the neighbours: stem cells and their niche. Cell, 116, 769-78. https://doi.org/10.1016/S0092-8674(04)00255-7
  29. Garozzo A, Cutrona D, Palmeri S, et al (1999). The role of p53 tumor suppressor gene as prognostic factor in laryngeal squamous cell carcinoma. Acta Otorhinolaryngol Ital, 19, 342-7.
  30. Ginestier C, Hur M, 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, 555-67. https://doi.org/10.1016/j.stem.2007.08.014
  31. Hermann P, Huber S, Herrler T, et al (2007). Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell, 1, 313-23. https://doi.org/10.1016/j.stem.2007.06.002
  32. Hirschmann-Jax C, Foster A, Wulf G, et al (2004). A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA, 101, 14228-33. https://doi.org/10.1073/pnas.0400067101
  33. Isacke C, Yarwood H (2002). The hyaluronan receptor, CD44. Int J Biochem Cell Biol, 34, 718-21. https://doi.org/10.1016/S1357-2725(01)00166-2
  34. Iwatsuki M, Mimori K, Yokobori T, et al (2010). Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci, 101, 293-9. https://doi.org/10.1111/j.1349-7006.2009.01419.x
  35. Jemal A, Bray F, Center M, et al (2011). Global cancer statistics. CA Cancer J Clin, 61, 69-90. https://doi.org/10.3322/caac.20107
  36. Joshua B, Kaplan M, Doweck I, et al (2012). Frequency of cells expressing CD44,ahead and neck cancer stem cell marker: correlation with tumor aggressiveness. Head Neck, 34, 42-9. https://doi.org/10.1002/hed.21699
  37. Kajita M, Itoh Y, Chiba T, et al (2001). Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol, 153, 893-904. https://doi.org/10.1083/jcb.153.5.893
  38. Kalluri R, Neilson E (2003). Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest, 112, 1776-84. https://doi.org/10.1172/JCI200320530
  39. Kalluri R, Weinberg R (2009). The basics of epithelial-mesenchymal transition. J Clin Invest, 119, 1420-8. https://doi.org/10.1172/JCI39104
  40. Koukourakis MI, Giatromanolaki A, Tsakmaki V, et al (2012). Cancer stem cell phenotype relates to radiochemotherapy out come in locally advanced squamous cell head-neck cancer. Br J Cancer, 106, 846-53. https://doi.org/10.1038/bjc.2012.33
  41. Krishnamurthy S, Dong Z, Vodopyanov D, et al (2010). Endothelial cell-initiated signalling promotes the survival and self renewal of cancer stem cells. Cancer Res, 70, 9969-78. https://doi.org/10.1158/0008-5472.CAN-10-1712
  42. Krishnamurthy S, Nor J (2012). Head and neck cancer stem cells. J Dent Res, 91, 334-40. https://doi.org/10.1177/0022034511423393
  43. Kuhn N, Tuan R (2010). Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J Cell Physiol, 222, 268-77. https://doi.org/10.1002/jcp.21940
  44. Li Q, Xu J, Wang W, et al (2009). Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clin Cancer Res, 15, 2657-65. https://doi.org/10.1158/1078-0432.CCR-08-2372
  45. Lim S, Oh S (2005). The role of CD24 in various human epithelial neoplasias. Pathol Res Pract, 201, 479-86. https://doi.org/10.1016/j.prp.2005.05.004
  46. Lim Y, Oh S, Cha Y, et al (2011). Cancer stem cell traits in squamospheres derived from primary head and neck squamous cell carcinomas. Oral Oncol, 47, 83-91. https://doi.org/10.1016/j.oraloncology.2010.11.011
  47. Mani S, Guo W, Liao M, et al (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell, 133, 704-15. https://doi.org/10.1016/j.cell.2008.03.027
  48. Morel A, Lievre M, Thomas C, et al (2008). Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One, 3, 2888. https://doi.org/10.1371/journal.pone.0002888
  49. Moreno-Bueno G, Portillo F, Cano A (2008). Transcriptional regulation of cell polarity in EMT and cancer. Oncogene, 27, 6958-69. https://doi.org/10.1038/onc.2008.346
  50. Morrison S, Spradling A (2008). Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life. Cell, 132, 598-611. https://doi.org/10.1016/j.cell.2008.01.038
  51. Neiva K, Zhang Z, Miyazawa M, et al (2009). Crosstalk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells through STAT/Akt/ERK signaling. Neoplasia, 11, 583-93.
  52. Nor J, Peters M, Christensen J, et al (2001). Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Invest, 81, 453-63. https://doi.org/10.1038/labinvest.3780253
  53. Nowell P (1976). The clonal evolution of tumor cell populations. Science, 194, 23-8 https://doi.org/10.1126/science.959840
  54. Okamoto A, Chikamatsu K, Sakakura K, et al (2009). Expansion and characterization of cancer stem-like cells in squamous cell carcinoma of the head and neck. Oral Oncol, 45, 633-9. https://doi.org/10.1016/j.oraloncology.2008.10.003
  55. Park I, Morrison S, Clarke M (2004). Bmi-1, stem cells, and senescence regulation. J Clin Invest, 113, 175-9. https://doi.org/10.1172/JCI200420800
  56. Perl A, Wilgenbus P, Dahl U, et al (1998). A causal role for Ecadherin in the transition from adenoma to carcinoma. Nature, 392, 190-3. https://doi.org/10.1038/32433
  57. Pierce G, Dixon F, Verney E (1960). Teratocarcinogenic and tissue forming potentials of the cell types comprising neoplastic embryoid bodies. Lab Invest, 9, 583-602.
  58. Prince M, Ailles L (2008). Cancer stem cells in head and neck squamous cell cancer. J Clin Oncol, 26, 2871-5. https://doi.org/10.1200/JCO.2007.15.1613
  59. Prince M, Sivanandan R, Kaczorowski A, 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 USA, 104, 973-8. https://doi.org/10.1073/pnas.0610117104
  60. Reya T, Morrison S, Clarke M, et al (2001). Stem cells, cancer, and cancer stem cells. Nature, 414, 105-11. https://doi.org/10.1038/35102167
  61. Radisky D, LaBarge M (2008). Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell, 2, 511-2. https://doi.org/10.1016/j.stem.2008.05.007
  62. Rasper M, Schafer A, Piontek G, et al (2010). Aldehyde dehydrogenase 1 positive glioblastoma cells show brain tumor stem cell capacity. Neuro Oncol, 12, 1024-33. https://doi.org/10.1093/neuonc/noq070
  63. Sanchez-Tillo E, Lazaro A, Torrent R, et al (2010). ZEB1 represses E-cadherin and induces an EMT by recruiting the SWI/ SNF chromatin-remodeling protein BRG1. Oncogene, 29, 3490-500. https://doi.org/10.1038/onc.2010.102
  64. Singh S, Hawkins C, Clarke I, et al (2004). Identification of human brain tumour initiating cells. Nature, 432, 396-401. https://doi.org/10.1038/nature03128
  65. Shook D, Keller R (2003). Mechanisms, mechanics and function of epithelialmesenchymal transition in early development. Mech Dev, 120, 1351-83. https://doi.org/10.1016/j.mod.2003.06.005
  66. Spivakov M, Fisher A (2007). Epigenetic signatures of stem-cell identity. Nat Rev Cancer, 8, 263-71. https://doi.org/10.1038/nrg2046
  67. Sun S, Wang Z (2011). Head neck squamous cell carcinoma c-Met+ cells display cancer stem cell properties and are responsible for cisplatin-resistance and metastasis. Int J Cancer, 129, 2337-48. https://doi.org/10.1002/ijc.25927
  68. Thiery J (2002). Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer, 2, 442-54. https://doi.org/10.1038/nrc822
  69. Thiery J, Acloque H, YJ Huang R, et al (2009). Epithelial-mesenchymal transitions in development and disease. Cell, 139, 871-90. https://doi.org/10.1016/j.cell.2009.11.007
  70. Thomasson H, Edenberg H, Crabb D, et al (1991). Alcohol and aldehyde dehydrogenase genotypes and alcoholism in Chinese men. Am J Hum Genet, 148, 677-81.
  71. Till J, McCulloch E (1961). A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res, 14, 213-22. https://doi.org/10.2307/3570892
  72. Valk-lingbeek M, Bruggeman S, Van Lohuizen M (2004). Stem cells and cancer; the polycomb connection. Cell, 118, 409-18. https://doi.org/10.1016/j.cell.2004.08.005
  73. Vlashi E, McBride W, Pajonk, F (2009). Radiation responses of cancer stem cells. J Cell Biochem, 108, 339-42. https://doi.org/10.1002/jcb.22275
  74. Visus C, Ito D, Amoscato A, et al (2007). 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, 67, 10538-45. https://doi.org/10.1158/0008-5472.CAN-07-1346
  75. Visvader J, Lindeman G (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer, 8, 755-68. https://doi.org/10.1038/nrc2499
  76. Wang S, Wong G, de Heer A, et al (2009). CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope, 119, 1518-30. https://doi.org/10.1002/lary.20506
  77. Whiteman E, Liu C, Fearon E, et al (2008). The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene, 27, 3875-9. https://doi.org/10.1038/onc.2008.9
  78. Widschwendter M, Fiegl H, Egle D, et al (2007). Epigenetic stem cell signature in cancer. Nat Genet, 39, 157-8. https://doi.org/10.1038/ng1941
  79. Wollenberg B (2011). Implication of stem cells in the biology and therapy of head and neck cancer. GMS Curr Top Otolaryngol Head Neck Surg, 10.
  80. Xia H, Cheung WK, Sze J, et al (2010). MiR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and ${\beta}$-catenin signaling. J Biol Chem, 285, 36995-7004. https://doi.org/10.1074/jbc.M110.133744
  81. Yang A, Fan F, Camp E (2006). Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res, 12, 4147-53. https://doi.org/10.1158/1078-0432.CCR-06-0038
  82. Yang J, Mani S, Donaher J, et al (2004). Twist a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell, 117, 927-39. https://doi.org/10.1016/j.cell.2004.06.006
  83. Yang M, Wu M, Chiou S, et al (2008). Direct regulation of TWIST by HIF-1a promotes metastasis. Nat Cell Biol, 10, 295-305. https://doi.org/10.1038/ncb1691
  84. Yang M, Hsu D, Wang H, et al (2010). Bmi-1 is essential in twist1-induced epithelial-mesenchymal transition. Nat Cell Biol, 12, 982-92. https://doi.org/10.1038/ncb2099
  85. Zhang P, Zhang Y, Mao L, et al (2009). Side population in oral squamous cell carcinoma possesses tumor stem cell phenotypes. Cancer Lett, 277, 227-34. https://doi.org/10.1016/j.canlet.2008.12.015
  86. Zhang Q, Shi S, Yen Y, et al (2010). A subpopulation of CD133(+) cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett, 289, 151-60. https://doi.org/10.1016/j.canlet.2009.08.010
  87. Zhang Z, Neiva K, Lingen M, et al (2010). VEGF-dependent tumor angiogenesis requires inverse and reciprocal regulation of VEGFR1 and VEGFR2. Cell Death Differ, 17, 499-512. https://doi.org/10.1038/cdd.2009.152
  88. Zhang Z, Filho M, Nor J (2012). The biology of head and neck cancer stem cells. Oral Oncol, 48, 1-9. https://doi.org/10.1016/j.oraloncology.2011.10.004
  89. Zhou L, Wei X, Cheng L, et al (2007). CD133,one of the markers of cancer stem cells in Hep-2cell line. Laryngoscope, 117, 455-60. https://doi.org/10.1097/01.mlg.0000251586.15299.35

Cited by

  1. ALDH1 in Combination with CD44 as Putative Cancer Stem Cell Markers are Correlated with Poor Prognosis in Urothelial Carcinoma of the Urinary Bladder vol.15, pp.5, 2014, https://doi.org/10.7314/APJCP.2014.15.5.2013
  2. MicroRNAs in Cervical Cancer: Evidences for a miRNA Profile Deregulated by HPV and Its Impact on Radio-Resistance vol.19, pp.5, 2014, https://doi.org/10.3390/molecules19056263
  3. Clinicopathological Significance of CD133 and ALDH1 Cancer Stem Cell Marker Expression in Invasive Ductal Breast Carcinoma vol.16, pp.17, 2015, https://doi.org/10.7314/APJCP.2015.16.17.7491
  4. The role of CD29-ILK-Akt signaling-mediated epithelial–mesenchymal transition of liver epithelial cells and chemoresistance and radioresistance in hepatocellular carcinoma cells vol.32, pp.5, 2015, https://doi.org/10.1007/s12032-015-0595-x
  5. Honokiol inhibits sphere formation and xenograft growth of oral cancer side population cells accompanied with JAK/STAT signaling pathway suppression and apoptosis induction vol.16, pp.1, 2016, https://doi.org/10.1186/s12885-016-2265-6
  6. The upregulated α-catulin expression was involved in head-neck squamous cell carcinogenesis by promoting proliferation, migration, invasion, and epithelial to mesenchymal transition vol.37, pp.2, 2016, https://doi.org/10.1007/s13277-015-3901-5
  7. Prognostic Value of Cancer Stem Cell Markers in Head and Neck Squamous Cell Carcinoma: a Meta-analysis vol.7, pp.2045-2322, 2017, https://doi.org/10.1038/srep43008
  8. Increased expression of CD44 is associated with more aggressive behavior in clear cell renal cell carcinoma vol.12, pp.1, 2018, https://doi.org/10.2217/bmm-2017-0142
  9. Influence of CD133+ expression on patients' survival and resistance of CD133+ cells to anti-tumor reagents in gastric cancer vol.5, pp.12, 2015, https://doi.org/10.1016/j.apjtb.2015.09.005
  10. The Epithelial-to-Mesenchymal Transition-Like Process in Glioblastoma: An Updated Systematic Review and In Silico Investigation vol.37, pp.2, 2016, https://doi.org/10.1002/med.21408
  11. The promise of stem cell markers in the diagnosis and therapy of epithelial dysplasia and oral squamous cell carcinoma vol.233, pp.11, 2018, https://doi.org/10.1002/jcp.26789