RhoC regulates cancer stem cells in head and neck squamous cell carcinoma by overexpressing IL-6 and phosphorylation of STAT3

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Islam, Mozaffarul ^a,b   Sharma, Smita ^b   Teknos, Theodoros N ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; HERMES ANTIGEN; INTERLEUKIN 6; OCTAMER TRANSCRIPTION FACTOR 4; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC PROTEIN; SHORT HAIRPIN RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; ALDEHYDE DEHYDROGENASE ISOENZYME 1; CD44 PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATE; IL6 PROTEIN, HUMAN; ISOENZYME; RETINAL DEHYDROGENASE; RHOC PROTEIN, HUMAN; SMALL INTERFERING RNA; STAT3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CANCER STEM CELL; CELL GROWTH; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; CHEMISTRY; GENE EXPRESSION REGULATION; HEAD AND NECK TUMOR; METABOLISM; PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ANTIGENS, CD44; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GUANOSINE TRIPHOSPHATE; HEAD AND NECK NEOPLASMS; HUMANS; INTERLEUKIN-6; ISOENZYMES; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; RETINAL DEHYDROGENASE; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS;

EID: 84895756231     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088527     Document Type: Article

References (48)

1. Parkin DM (2001) Global cancer statistics in the year 2000. Lancet Oncol 2: 533-543.
2. Leemans CR, Braakhuis BJ, Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nat Rev Cancer 11: 9-22.
3. ACS American Cancer Society: Cancer Facts and Figures, 2013, pp1-62.
4. Bjordal K, Kaasa S (1995) Psychological distress in head and neck cancer patients 7-11 years after curative treatment. Br J Cancer 71: 592-597.
5. Brown ML RG, Schussler N, Etzioni R (2002) Estimating health care costs related to cancer treatment from SEER-Medicare data. Med care 40[8 suppl]:IV-17.
6. Takes RP, Rinaldo A, Silver CE, Haigentz M, Jr., Woolgar JA, et al. (2012) Distant metastases from head and neck squamous cell carcinoma. Part I. Basic aspects. Oral Oncol 48: 775-779.
7. Yi JS, Kim JS, Lee JH, Choi SH, Nam SY, et al. (2012) 18F-FDG PET/CT for detecting distant metastases in patients with recurrent head and neck squamous cell carcinoma. J Surg Oncol 106: 708-712.
8. Sahai E, Marshall CJ (2002) RHO-GTPases and cancer. Nat Rev Cancer 2: 133-142.
9. Nobes CD, Hall A (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53-62.
10. Hakem A, Sanchez-Sweatman O, You-Ten A, Duncan G, Wakeham A, et al. (2005) RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev 19: 1974-1979. (Pubitemid 41247955)
11. van Golen KL, Wu ZF, Qiao XT, Bao L, Merajver SD (2000) RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia 2: 418-425. (Pubitemid 32044787)
12. Kleer CG, Teknos TN, Islam M, Marcus B, Lee JS, et al. (2006) RhoC GTPase expression as a potential marker of lymph node metastasis in squamous cell carcinomas of the head and neck. Clin Cancer Res 12: 4485-4490. (Pubitemid 44297796)
13. Islam M, Lin G, Brenner JC, Pan Q, Merajver SD, et al. (2009) RhoC Expression and Head and Neck Cancer Metastasis. Mol Cancer Res 7: 1771-1780.
14. van Golen KL, Wu ZF, Qiao XT, Bao LW, Merajver SD (2000) RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res 60: 5832-5838.
15. Hassan KA, Wang L, Korkaya H, Chen G, Maillard I, et al. (2013) Notch Pathway Activity Identifies Cells with Cancer Stem Cell-like Properties and Correlates with Worse Survival in Lung Adenocarcinoma. Clin Cancer Res.
16. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, 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 U S A 104: 973-978. (Pubitemid 46154721)
17. Mannelli G, Gallo O (2012) Cancer stem cells hypothesis and stem cells in head and neck cancers. Cancer Treat Rev 38: 515-539.
18. Davis SJ, Divi V, Owen JH, Bradford CR, Carey TE, et al. (2010) Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 136: 1260-1266.
19. Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, et al. (2010) Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck 32: 1195-1201.
20. Chen YW, Chen KH, Huang PI, Chen YC, Chiou GY, et al. (2010) Cucurbitacin I suppressed stem-like property and enhanced radiation-induced apoptosis in head and neck squamous carcinoma-derived CD44(+)ALDH1(+) cells. Mol Cancer Ther 9: 2879-2892.
21. 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.
22. Carey TE, Kimmel KA, Schwartz DR, Richter DE, Baker SR, et al. (1983) Antibodies to human squamous cell carcinoma. Otolaryngol Head Neck Surg 91: 482-491. (Pubitemid 14225421)
23. Krause CJ, Carey TE, Ott RW, Hurbis C, McClatchey KD, et al. (1981) Human squamous cell carcinoma. Establishment and characterization of new permanent cell lines. Arch Otolaryngol 107: 703-710. (Pubitemid 11027726)
24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
25. Islam M, Sharma S, Kumar B, Teknos TN (2013) Atorvastatin inhibits RhoC function and limits head and neck cancer metastasis. Oral Oncol 49: 778-786.
26. Mack B, Gires O (2008) CD44s and CD44v6 expression in head and neck epithelia. PLoS One 3: e3360.
27. Rosenthal DT, Zhang J, Bao L, Zhu L, Wu Z, et al. (2012) RhoC impacts the metastatic potential and abundance of breast cancer stem cells. PLoS One 7: e40979.
28. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, et al. (2005) Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25: 2475-2485. (Pubitemid 40354640)
29. Takao Y, Yokota T, Koide H (2007) Beta-catenin up-regulates Nanog expression through interaction with Oct-3/4 in embryonic stem cells. Biochem Biophys Res Commun 353: 699-705. (Pubitemid 46048726)
30. Gupta M, Han JJ, Stenson M, Wellik L, Witzig TE (2012) Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia 26: 1356-1364.
31. Gupta M, Maurer M, Wellik L (2012) Abstract 2576:103rd AACR Annual Meeting: STAT3 tyrosine phosphorylation is frequent in diffuse large B cell lymphoma and is independent of molecular subtype: Implications for biomarker. Cancer Res 72: supplement 1.
32. Takeda T, Kurachi H, Yamamoto T, Nishio Y, Nakatsuji Y, et al. (1998) Crosstalk between the interleukin-6 (IL-6)-JAK-STAT and the glucocorticoidnuclear receptor pathway: synergistic activation of IL-6 response element by IL-6 and glucocorticoid. J Endocrinol 159: 323-330. (Pubitemid 28520186)
33. Berishaj M, Gao SP, Ahmed S, Leslie K, Al-Ahmadie H, et al. (2007) Stat3 is tyrosine-phosphorylated through the interleukin-6/glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res 9: R32.
34. Duffy SA, Taylor JM, Terrell JE, Islam M, Li Y, et al. (2008) Interleukin-6 predicts recurrence and survival among head and neck cancer patients. Cancer 113: 750-757.
35. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P (2011) IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 9: 1658-1667.
36. Ikoma T, Takahashi T, Nagano S, Li YM, Ohno Y, et al. (2004) A definitive role of RhoC in metastasis of orthotopic lung cancer in mice. Clin Cancer Res 10: 1192-1200. (Pubitemid 38198921)
37. Schmalbach CE, Chepeha DB, Giordano TJ, Rubin MA, Teknos TN, et al. (2004) Molecular profiling and the identification of genes associated with metastatic oral cavity/pharynx squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 130: 295-302. (Pubitemid 38314227)
38. Huang CP, Tsai MF, Chang TH, Tang WC, Chen SY, et al. (2013) ALDH-positive lung cancer stem cells confer resistance to epidermal growth factor receptor tyrosine kinase inhibitors. Cancer Lett 328: 144-151.
39. Lohberger B, Rinner B, Stuendl N, Absenger M, Liegl-Atzwanger B, et al. (2012) Aldehyde dehydrogenase 1, a potential marker for cancer stem cells in human sarcoma. PLoS One 7: e43664.
40. 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. (Pubitemid 350056407)
41. Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, et al. (2011) Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 64: 937-946.
42. Collura A, Marisa L, Trojan D, Buhard O, Lagrange A, et al. (2012) Extensive characterization of sphere models established from colorectal cancer cell lines. Cell Mol Life Sci.
43. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, et al. (2009) Nanog is the gateway to the pluripotent ground state. Cell 138: 722-737.
44. Wang Z, Oron E, Nelson B, Razis S, Ivanova N (2012) Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell 10: 440-454.
45. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, et al. (2009) 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 18: 1093-1108.
46. Torres J, Watt FM (2008) Nanog maintains pluripotency of mouse embryonic stem cells by inhibiting NFkappaB and cooperating with Stat3. Nat Cell Biol 10: 194-201. (Pubitemid 351194049)
47. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, et al. (2001) Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 7: 1419-1428. (Pubitemid 32708698)
48. Liu CA, Wang MJ, Chi CW, Wu CW, Chen JY (2004) Rho/Rhotekin-mediated NF-kappaB activation confers resistance to apoptosis. Oncogene 23: 8731-8742.