Toll-like receptor 3 stimulation triggers metabolic reprogramming in pharyngeal cancer cell line through Myc, MAPK, and HIF

Molecular Carcinogenesis

Volumn 56, Issue 4, 2017, Pages 1214-1226

  Matijevic Glavan, Tanja ^a   Cipak Gasparovic, Ana ^a   Vérillaud, Benjamin ^b,c   Busson, Pierre ^b   Pavelic, Jasminka ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c HÔPITAL LARIBOISIÈRE   (France)

Author keywords

cell migration; metabolism; poly(A:U); poly(I:C); toll like receptor 3

Indexed keywords

CD44V ANTIGEN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; HYPOXIA INDUCIBLE FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; NUCLEAR PROTEIN; PHOSPHOTRANSFERASE; PYRUVATE KINASE M2; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; HYPOXIA INDUCIBLE FACTOR 1; POLYINOSINIC POLYCYTIDYLIC ACID; TLR3 PROTEIN, HUMAN;

AEROBIC GLYCOLYSIS; APOPTOSIS; ARTICLE; BIOLOGICAL FUNCTIONS; CELL MIGRATION; GENE OVEREXPRESSION; GLYCOLYSIS; HEAD AND NECK CANCER CELL LINE; HUMAN; HUMAN CELL; METABOLIC REPROGRAMMING; PHARYNX CANCER; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; UPREGULATION; CELL MOTION; MAPK SIGNALING; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PHARYNX; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; MAP KINASE SIGNALING SYSTEM; OXIDATIVE STRESS; PHARYNGEAL NEOPLASMS; PHARYNX; POLY I-C; PROTO-ONCOGENE PROTEINS C-MYC; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 85004001432     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22584     Document Type: Article

References (48)

1. Huang B, Zhao J, Li H, et al. Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res 2005; 65:5009–5014.
2. Kelly MG, Alvero AB, Chen R, et al. TLR-4 signaling promotes tumor growth and paclitaxel chemoresistance in ovarian cancer. Cancer Res 2006; 66:3859–3868.
3. Huang B, Zhao J, Shen S, et al. Listeria monocytogenes promotes tumor growth via tumor cell toll-like receptor 2 signaling. Cancer Res 2007; 67:4346–4352.
4. Huang B, Zhao J, Unkeless JC, Feng ZH, Xiong H. TLR signaling by tumor and immune cells: A double-edged sword. Oncogene 2008; 27:218–224.
5. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D. MRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004; 279:12542–12550.
6. Matijevic T, Pavelic J. The dual role of TLR3 in metastatic cell line. Clin Exp Metastasis 2011; 28:701–712.
7. Rydberg C, Mansson A, Uddman R, Riesbeck K, Cardell LO. Toll-like receptor agonists induce inflammation and cell death in a model of head and neck squamous cell carcinomas. Immunology 2009; 128:600–611.
8. Pries R, Hogrefe L, Xie L, et al. Induction of c-Myc-dependent cell proliferation through toll-like receptor 3 in head and neck cancer. Int J Mol Med 2008; 21:209–215.
9. Fernandez-Garcia B, Eiró N, González-Reyes S, et al. Clinical significance of toll-like receptor 3, 4, and 9 in gastric cancer. J Immunother 2014; 37:77–83.
10. González-Reyes S, Marín L, González L, et al. Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer 2010; 10:665.
11. González-Reyes S, Fernández JM, González LO, et al. Study of TLR3, TLR4, and TLR9 in prostate carcinomas and their association with biochemical recurrence. Cancer Immunol Immunother 2011; 60:217–226.
12. Paone A, Galli R, Gabellini C, et al. Toll-like receptor 3 regulates angiogenesis and apoptosis in prostate cancer cell lines through hypoxia-inducible factor 1 alpha. Neoplasia 2010; 12:539–549.
13. Thuringer D, Jego G, Wettstein G, et al. Extracellular HSP27 mediates angiogenesis through toll-like receptor 3. Faseb J 2013; 27:4169–4183.
14. Matijevic T, Pavelic J. Poly(I:C) treatment influences the expression of calreticulin and profilin-1 in a human HNSCC cell line: A proteomic study. Tumour Biol 2012; 33:1201–1208.
15. Perrot I, Deauvieau F, Massacrier C, et al. TLR3 and Rig-like receptor on myeloid dendritic cells and Rig-like receptor on human NK cells are both mandatory for production of IFN-gamma in response to double-stranded RNA. J Immunol 2010; 185:2080–2088.
16. Kalinich JF, Ramakrishnan N, McClain DE. The antioxidant Trolox enhances the oxidation of 2′,7′-dichlorofluorescin to 2′,7′-dichlorofluorescein. Free Radic Res 1997; 26:37–47.
17. Goth L. A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 1991; 196:143–151.
18. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Anal Biochem 1969; 27:502–522.
19. Zou C, Wang Y, Shen Z. 2-NBDG as a fluorescent indicator for direct glucose uptake measurement. J Biochem Biophys Methods 2005; 64:207–215.
20. Chuang HC, Huang CC, Chien CY, Chuang JH. Toll-like receptor 3-mediated tumor invasion in head and neck cancer. Oral Oncol 2012; 48:226–232.
21. McCall KD, Harii N, Lewis CJ, et al. High basal levels of functional toll-like receptor 3 (TLR3) and noncanonical Wnt5a are expressed in papillary thyroid cancer and are coordinately decreased by phenylmethimazole together with cell proliferation and migration. Endocrinology 2007; 148:4226–4237.
22. Schwartz AL, Malgor R, Dickerson E, et al. Phenylmethimazole decreases Toll-like receptor 3 and noncanonical Wnt5a expression in pancreatic cancer and melanoma together with tumor cell growth and migration. Clin Cancer Res 2009; 15:4114–4122.
23. David CJ, Chen M, Assanah M, Canoll P, Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010; 463:364–368.
24. Li JZ, Gao W, Chan JY, Ho WK, Wong TS. Hypoxia in head and neck squamous cell carcinoma. ISRN Otolaryngol 2012;708974.
25. Taelman VF, Dobrowolski R, Plouhinec JL, et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010; 143:1136–1148.
26. McCall KD, Harii N, Lewis CJ, et al. High basal levels of functional toll-like receptor 3 (TLR3) and noncanonical Wnt5a are expressed in papillary thyroid cancer and are coordinately decreased by phenylmethimazole together with cell proliferation and migration. Endocrinology 2007; 148:4226–4237.
27. Du Q, Geller DA. Cross-regulation between Wnt and NF-kappaB signaling pathways. For Immunopathol Dis Therap 2010; 1:155–181.
28. Matter N, Marx M, Weg-Remers S, Ponta H, Herrlich P, Konig H. Heterogeneous ribonucleoprotein A1 is part of an exon-specific splice-silencing complex controlled by oncogenic signaling pathways. J Biol Chem 2000; 275:35353–35360.
29. Assimakopoulos D, Kolettas E, Patrikakos G, Evangelou A. The role of CD44 in the development and prognosis of head and neck squamous cell carcinomas. Histol Histopathol 2002; 17:1269–1281.
30. Zhou ZJ, Dai Z, Zhou SL, et al. Overexpression of HnRNP A1 promotes tumor invasion through regulating CD44v6 and indicates poor prognosis for hepatocellular carcinoma. Int J Cancer 2013; 132:1080–1089.
31. Iida N, Bourguignon LY. Coexpression of CD44 variant (v10/ex14) and CD44S in human mammary epithelial cells promotes tumorigenesis. J Cell Physiol 1997; 171:152–160.
32. Kan M, Aki M, Akiyama K, Naruo S, Kanayama H, Kagawa S. High-level expression of the CD44 variant sharing exon v10 in renal cancer. Jpn J Cancer Res 1995; 86:847–853.
33. Iida J, Clancy R, Dorchak J, et al. DNA aptamers against exon v10 of CD44 inhibit breast cancer cell migration. PLoS ONE 2014; 9:e88712.
34. Yoshinari C, Mizusawa N, Byers HR, Akasaka T. CD44 variant isoform CD44v10 expression of human melanoma cell lines is upregulated by hyaluronate and correlates with migration. Melanoma Res 1999; 9:223–231.
35. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis 2013; 4:532.
36. Storz P. Reactive oxygen species in tumor progression. Front Biosci 2005; 10:1881–1896.
37. Kundu N, Zhang S, Fulton AM. Sublethal oxidative stress inhibits tumor cell adhesion and enhances experimental metastasis of murine mammary carcinoma. Clin Exp Metastasis 1995; 13:16–22.
38. Pelicano H, Lu W, Zhou Y, et al. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res 2009; 69:2375–2383.
39. Hitchler MJ, Oberley LW, Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 2008; 45:1573–1580.
40. Courtnay R, Ngo DC, Malik N, et al. Cancer metabolism and the Warburg effect: The role of HIF-1 and PI3K. Mol Biol Rep 2015; 42:841–851.
41. Miyamoto S, Murphy AN, Brown JH. Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ 2008; 15:521–529.
42. Tamada M, Nagano O, Tateyama S, et al. Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells. Cancer Res 2012; 72:1438–1448.
43. Luo W, Hu H, Chang R, et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 2011; 145:732–744.
44. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ 2007; 14:400–410.
45. Marampon F, Ciccarelli C, Zani BM. Down-regulation of c-Myc following MEK/ERK inhibition halts the expression of malignant phenotype in rhabdomyosarcoma and in non muscle-derived human tumors. Mol Cancer 2006; 5:31.
46. Miller DM, Thomas SD, Islam A, Muench D, Sedoris K. C-Myc and cancer metabolism. Clin Cancer Res 2012; 18:5546–5553.
47. Dang CV, Le A, Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin Cancer Res 2009; 15:6479–6483.
48. Glavan TM, Pavelic J. The exploitation of toll-like receptor 3 signaling in cancer therapy. Curr Pharm Des 2014; 20:6555–6564.