Molecular characterization and clinical implications of spindle cells in nasopharyngeal carcinoma: A novel molecule-morphology model of tumor progression proposed

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Luo, Weiren ^a   Yao, Kaitai ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE ISOENZYME 1; BETA CATENIN; BREAST CANCER RESISTANCE PROTEIN; FIBRONECTIN; GELATINASE A; LATENT MEMBRANE PROTEIN 1; NERVE CELL ADHESION MOLECULE; OSTEONECTIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UVOMORULIN; TUMOR MARKER; TUMOR PROTEIN;

ARTICLE; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STEM CELL; CANCER SURVIVAL; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; METASTASIS POTENTIAL; NASOPHARYNX CARCINOMA; SPINDLE CELL; TUMOR GROWTH; UPREGULATION; BIOLOGICAL MODEL; BIOSYNTHESIS; CLINICAL TRIAL; DISEASE FREE SURVIVAL; FEMALE; FOLLOW UP; MALE; METABOLISM; MORTALITY; NASOPHARYNX TUMOR; PATHOLOGY; RETROSPECTIVE STUDY; SURVIVAL RATE;

DISEASE-FREE SURVIVAL; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MODELS, BIOLOGICAL; NASOPHARYNGEAL NEOPLASMS; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; RETROSPECTIVE STUDIES; SURVIVAL RATE; TUMOR MARKERS, BIOLOGICAL;

EID: 84892569943     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083135     Document Type: Article

References (56)

1. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890. doi:10.1016/j.cell. 2009.11.007. PubMed: 19945376.
2. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nature Rev Cancer 2: 442-454. doi:10.1038/nrc822.
3. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428. doi:10.1172/JCI39104. PubMed: 19487818.
4. Gupta PB, Chaffer CL, Weinberg RA (2009) Cancer stem cells: mirage or reality? Nat Med 15: 1010-1012. doi:10.1038/nm0909-1010. PubMed: 19734877.
5. Clevers H (2011) The cancer stem cell: premises, promises and challenges. Nat Med 17: 313-319. PubMed: 21386835.
6. Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273. doi:10.1038/nrc2620. PubMed: 19262571.
7. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715. doi:10.1016/j.cell.2008.03.027. PubMed: 18485877.
8. Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y et al. (2011) p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 13: 317-323. doi:10.1038/ncb2173. PubMed: 21336307.
9. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005) Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat Rev Cancer 5: 744-749. doi:10.1038/nrc1694. PubMed: 16148886.
10. Jemal A, Bray F, Center MM, Ferlay J, Ward E et al. (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90. doi:10.3322/caac.20107. PubMed: 21296855.
11. Zhang L, Zhu YX, Wang Y, Huang CP, Wu Y et al. (2011) Salvage surgery for neck residue or recurrence of nasopharyngeal carcinoma: a 10-year experience. Ann Surg Oncol 18: 233-238. doi:10.1245/s10434-010-1498-x. PubMed: 20737217.
12. Razak AR, Siu LL, Liu FF, Ito E, O'Sullivan B et al. (2010) Nasopharyngeal carcinoma: the next challenges. Eur J Cancer 46: 1967-1978. doi:10.1016/j.ejca.2010.04.004. PubMed: 20451372.
13. Wei WI, Sham JS (2005) Nasopharyngeal carcinoma. Lancet 365: 2041-2054. doi:10.1016/S0140-6736(05)66698-6. PubMed: 15950718.
14. Chen MH, Zong YS (1992) Morphometric features of small spindle cell carcinoma in the nasopharynx. Clin Exp Pathol 8: 179-181.
15. Thompson L (2006) World Health Organization classification of tumours: pathology and genetics of head and neck tumours. Ear Nose Throat J 85: 74. PubMed: 16579185.
16. Luo WR, Chen XY, Li SY, Wu AB, Yao KT (2012) Neoplastic spindle cells in nasopharyngeal carcinoma show features of epithelialmesenchymal transition. Histopathology 61: 113-122. doi:10.1111/j.1365-2559.2012.04205.x. PubMed: 22486228.
17. Liang PC, Ch'en CC, Chu CC, Chu YF, Hu HM et al. (1962) The histopathologic classification, biologic characteristics and histogenesis of nasopharyngeal carcinomas. Chin Med J 81: 629-658. PubMed: 13930424. Available online at: PubMed: 13930424
18. Luo W, Fang W, Li S, Yao K (2012) Aberrant expression of nuclear vimentin and related epithelial-mesenchymal transition markers in nasopharyngeal carcinoma. Int J Cancer 131: 1863-1873. doi:10.1002/ijc.27467. PubMed: 22307379.
19. Li J, Guan HY, Gong LY, Song LB, Zhang N et al. (2008) Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res 14: 6996-7003. doi:10.1158/1078-0432.CCR-08-0754. PubMed: 18980995.
20. Liu Z, Kakudo K, Bai Y, Li Y, Ozaki T et al. (2011) Loss of cellular polarity/cohesiveness in the invasive front of papillary thyroid carcinoma, a novel predictor for lymph node metastasis; possible morphological indicator of epithelial mesenchymal transition. J Clin Pathol 64: 325-329. doi:10.1136/jcp.2010.083956. PubMed: 21296795.
21. Xia H, Cheung WK, Sze J, Lu G, Jiang S et al. (2010) miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and beta-catenin signaling. J Biol Chem 285: 36995-37004. doi:10.1074/jbc.M110.133744. PubMed: 20826811.
22. Wu AB, Luo WR, Zhang QB, Yang ZX, Zhang G et al. (2013) Aldehyde dehydrogenase 1, a functional marker for identifying cancer stem cells in human nasopharyngeal carcinoma. Cancer Lett 330: 181-189. doi:10.1016/j.canlet.2012. 11.046. PubMed: 23220285.
23. Niedobitek G, Hansmann ML, Herbst H, Young LS, Dienemann D et al. (1991) Epstein-Barr virus and carcinomas: undifferentiated carcinomas but not squamous cell carcinomas of the nasopharynx are regularly associated with the virus. J Pathol 165: 17-24. doi:10.1002/path.1711650105. PubMed: 1659626.
24. Niedobitek G, Agathanggelou A, Barber P, Smallman LA, Jones EL et al. (1993) P53 overexpression and Epstein-Barr virus infection in undifferentiated and squamous cell nasopharyngeal carcinomas. J Pathol 170: 457-461. doi:10.1002/path.1711700409. PubMed: 8410495.
25. Niedobitek G (2000) Epstein-Barr virus infection in the pathogenesis of nasopharyngeal carcinoma. Mol Pathol 53: 248-254. doi:10.1136/mp.53.5.248. PubMed: 11091848.
26. Luo WR, Gao F, Li SY, Yao KT (2012) Tumour budding and the expression of cancer stem cell marker aldehyde dehydrogenase 1 in nasopharyngeal carcinoma. Histopathology 61: 1072-1081. doi:10.1111/j.1365-2559.2012.04350.x. PubMed: 23020521.
27. Kononen J, Bubendorf L, Kallioniemi A, Bärlund M, Schraml P et al. (1998) Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 4: 844-847. doi:10.1038/nm0798-844. PubMed: 9662379.
28. Camp RL, Neumeister V, Rimm DL (2008) A decade of tissue microarrays: progress in the discovery and validation of cancer biomarkers. J Clin Oncol 26: 5630-5637. doi:10.1200/JCO.2008.17.3567. PubMed: 18936473.
29. Sarrió D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G et al. (2008) Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 68: 989-997. doi:10.1158/0008-5472.CAN-07- 2017. PubMed: 18281472.
30. Vallejos CS, Gómez HL, Cruz WR, Pinto JA, Dyer RR et al. (2010) Breast cancer classification according to immunohistochemistry markers: subtypes and association with clinicopathologic variables in a peruvian hospital database. Clin Breast Cancer 10: 294-300. doi:10.3816/CBC.2010.n.038. PubMed: 20705562.
31. Hassan KA, Chen G, Kalemkerian GP, Wicha MS, Beer DG (2009) An embryonic stem cell-like signature identifies poorly differentiated lung adenocarcinoma but not squamous cell carcinoma. Clin Cancer Res 15: 6386-6390. doi:10.1158/1078-0432.CCR-09-1105. PubMed: 19808871.
32. 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.
33. 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.
34. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037. doi:10.1158/0008-5472.CAN-06-2030. PubMed: 17283135.
35. 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.
36. Li T, Su Y, Mei Y, Leng Q, Leng B et al. (2010) ALDH1A1 is a marker for malignant Prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 90: 234-244. doi:10.1038/labinvest.2009.127. PubMed: 20010854.
37. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G et al. (2009) Aldehydedehydrogenase1 Is a marker for normal and malignant human colonic stem cells (SC) and tracks SC Cover population during colon tumorigenesis. Cancer Res 69: 3382-3389. doi:10.1158/0008-5472.CAN-08-4418. PubMed: 19336570.
38. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S et al. (2012) Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene 31: 1354-1365. doi:10.1038/onc.2011.338. PubMed: 21822303.
39. Kumar SM, Liu S, Lu H, Zhang H, Zhang PJ et al. (2012) Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene 31: 4898-4911. doi:10.1038/onc.2011.656. PubMed: 22286766.
40. Jeter CR, Liu B, Liu X, Chen X, Liu C et al. (2011) NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene 30: 3833-3845. doi:10.1038/onc.2011.114. PubMed: 21499299.
41. Park SY, Lee HE, Li H, Shipitsin M, Gelman R et al. (2010) Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 16: 876-887. doi:10.1158/1078-0432.CCR-09-1532. PubMed: 20103682.
42. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M et al. (2010) Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73. doi:10.1016/j.cell.2009.12.007. PubMed: 20074520.
43. Harn HJ, Hsieh HF, Ho LI, Yu CP, Chen JH et al. (1998) Apoptosis in nasopharyngeal carcinoma as related to histopathological characteristics and clinical stage. Histopathology 33: 117-122. doi:10.1046/j.1365-2559.1998.00470. x. PubMed: 9762543.
44. Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA (2007) A switch from E-cadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin Cancer Res 13: 7003-7011. doi:10.1158/1078-0432.CCR-07- 1263. PubMed: 18056176.
45. Nakajima S, Doi R, Toyoda E, Tsuji S, Wada M, et al. (2004). N-cadherin expression and epithelial-mesenchymal transition in pancreatic carcinoma. Clin Cancer Res 10: 4125-4133.
46. Satelli A, Li S (2011) Vimentin in cancer and its potential as a molecular target for cancer therapy. Cell Mol Life Sci 68: 3033-3046. doi:10.1007/s00018-011-0735-1. PubMed: 21637948.
47. 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.
48. Senba M, Zhong XY, Senba MI, Itakura H (1994) EBV and nasopharyngeal carcinoma. Lancet 343: 1104. doi:10.1016/S0140-6736(94)90218-6. PubMed: 7909127.
49. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I et al. (2007) Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67: 1970-1978. doi:10.1158/0008-5472.CAN-06-3933. PubMed: 17332324.
50. Horikawa T, Yoshizaki T, Kondo S, Furukawa M, Kaizaki Y et al. (2011) Epstein-Barr Virus latent membrane protein 1 induces Snail and epithelial-mesenchymal transition in metastatic nasopharyngeal carcinoma. Br J Cancer 104: 1160-1167. doi:10.1038/bjc.2011.38. PubMed: 21386845.
51. Kondo S, Wakisaka N, Muramatsu M, Zen Y, Endo K et al. (2011) Epstein-Barr virus latent membrane protein 1 induces cancer stem/progenitor-like cells in nasopharyngeal epithelial cell lines. J Virol 85: 11255-11264. doi:10.1128/JVI.00188-11. PubMed: 21849440.
52. Chan AT (2010) Nasopharyngeal carcinoma. Ann Oncol 21(Suppl 7): vii308-vii312. PubMed: 20943634.
53. Luo W, Li S, Peng B, Ye Y, Deng X et al. (2013) Embryonic stem cells markers SOX2, OCT4 and Nanog expression and their correlations with epithelial-mesenchymal transition in nasopharyngeal carcinoma. PLOS ONE 8: e56324. doi:10.1371/journal.pone.0056324. PubMed: 23424657.
54. Luo WR, Yao KT (2013) Cancer stem cell characteristics, ALDH1 expression in the invasive front of nasopharyngeal carcinoma. Virchows Arch. doi:10.1007/s00428-013-1508-z. PubMed: 24248285.
55. Li XJ, Peng LX, Shao JY, Lu WH, Zhang JX et al. (2012) As an independent unfavorable prognostic factor, IL-8 promotes metastasis of nasopharyngeal carcinoma through induction of epithelial-mesenchymal transition and activation of AKT signaling. Carcinogenesis 33: 1302-1309. doi:10.1093/carcin/bgs181. PubMed: 22610073.
56. Luo WR, Li LX, Li SY, Jiang HG, Chen XY (2010) Influence of celecoxib on invasiveness of human high-metastatic nasopharyngeal carcinoma cell line CNE-2Z. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 45: 941-945. PubMed: 21215211.