The noninflammatory role of high mobility group box 1/toll-like receptor 2 axis in the self-renewal of mammary cancer stem cells

FASEB Journal

Volumn 27, Issue 12, 2013, Pages 4731-4744

  Conti, Laura ^a   Lanzardo, Stefania ^a   Arigoni, Maddalena ^a   Antonazzo, Roberta ^a   Radaelli, Enrico ^b,c   Cantarella, Daniela ^d   Calogero, Raffaele A ^a   Cavallo, Federica ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b Mouse and Animal Pathology Lab   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d CANDIOLO CANCER INSTITUTE   (Italy)

Author keywords

BOXA; Breast carcinoma; Endogenous TLR2 ligands; MyD88; NFB; Transcriptome

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; SMAD3 PROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION;

BOXA; BREAST CARCINOMA; ENDOGENOUS TLR2 LIGANDS; MYD88; NFΚB; TRANSCRIPTOME;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL PROLIFERATION; FEMALE; HMGB1 PROTEIN; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-6; LUNG NEOPLASMS; MCF-7 CELLS; MICE; MICE, INBRED BALB C; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; SMAD3 PROTEIN; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 2; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84890540571     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-230201     Document Type: Article

References (40)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
2. Paul, S. M., Mytelka, D. S., Dunwiddie, C. T., Persinger, C. C., Munos, B. H., Lindborg, S. R., and Schacht, A. L. (2010) How to improve R&D productivity: the pharmaceutical industry's grand challenge. Nat. Rev. Drug Discov. 9, 203-214
3. Magee, J. A., Piskounova, E., and Morrison, S. J. (2012) Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 21, 283-296
4. Wicha, M. S., Liu, S., and Dontu, G. (2006) Cancer stem cells: an old idea-A paradigm shift. Cancer Res. 66, 1883-1890
5. Frank, N. Y., Schatton, T., and Frank, M. H. (2010) The therapeutic promise of the cancer stem cell concept. J. Clin. Inv. 120, 41-50
6. Noh, K. H., Lee, Y. H., Jeon, J. H., Kang, T. H., Mao, C. P., Wu, T. C., and Kim, T. W. (2012) Cancer vaccination drives Nanogdependent evolution of tumor cells toward an immune-resistant and stem-like phenotype. Cancer Res. 72, 1717-1727
7. Grange, C., Lanzardo, S., Cavallo, F., Camussi, G., and Bussolati, B. (2008) Sca-1 identifies the tumor-initiating cells in mammary tumors of BALB-neuT transgenic mice. Neoplasia 10, 1433-1443
8. Rovero, S., Boggio, K., Di Carlo, E., Amici, A., Quaglino, E., Porcedda, P., Musiani, P., and Forni, G. (2001) Insertion of the DNA for the 163-171 peptide of IL1beta enables a DNA vaccine encoding p185(neu) to inhibit mammary carcinogenesis in Her-2/neu transgenic BALB/c mice. Gene Ther. 8, 447-452
9. Boggio, K., Nicoletti, G., Di Carlo, E., Cavallo, F., Landuzzi, L., Melani, C., Giovarelli, M., Rossi, I., Nanni, P., De Giovanni, C., Bouchard, P., Wolf, S., Modesti, A., Musiani, P., Lollini, P. L., Colombo, M. P., and Forni, G. (1998) Interleukin 12-mediated prevention of spontaneous mammary adenocarcinomas in two lines of Her-2/neu transgenic mice. J. Exp. Med. 188, 589-596
10. Ponti, D., Costa, A., Zaffaroni, N., Pratesi, G., Petrangolini, G., Coradini, D., Pilotti, S., Pierotti, M. A., and Daidone, M. G. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65, 5506-5511
11. Sanges, R., Cordero, F., and Calogero, R. A. (2007) oneChannelGUI: a graphical interface to Bioconductor tools, designed for life scientists who are not familiar with R language. Bioinformatics. 23, 3406-3408
12. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 19, 185-193
13. Parmigiani, G., Garrett-Mayer, E. S., Anbazhagan, R., and Gabrielson, E. (2004) A cross-study comparison of gene expression studies for the molecular classification of lung cancer. Clin. Cancer Res. 10, 2922-2927
14. Smyth, G. K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3
15. Bookout, A. L., and Mangelsdorf, D. J. (2003) Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl. Recept. Signal. 1, e012
16. Cho, R. W., Wang, X., Diehn, M., Shedden, K., Chen, G. Y., Sherlock, G., Gurney, A., Lewicki, J., and Clarke, M. F. (2008) Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells 26, 364-371
17. Okano, H., Kawahara, H., Toriya, M., Nakao, K., Shibata, S., and Imai, T. (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp. Cell Res. 306, 349-356
18. Charafe-Jauffret, E., Ginestier, C., Iovino, F., Wicinski, J., Cervera, N., Finetti, P., Hur, M. H., Diebel, M. E., Monville, F., Dutcher, J., Brown, M., Viens, P., Xerri, L., Bertucci, F., Stassi, G., Dontu, G., Birnbaum, D., and Wicha, M. S. (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 69, 1302-1313
19. Jeter, C. R., Liu, B., Liu, X., Chen, X., Liu, C., Calhoun-Davis, T., Repass, J., Zaehres, H., Shen, J. J., and Tang, D. G. (2011) NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene 30, 3833-3845
20. Sallustio, F., De Benedictis, L., Castellano, G., Zaza, G., Loverre, A., Costantino, V., Grandaliano, G., and Schena, F. P. (2010) TLR2 plays a role in the activation of human resident renal stem/progenitor cells. FASEB J. 24, 514-525
21. Taylor, T., Kim, Y. J., Ou, X., Derbigny, W., and Broxmeyer, H. E. (2010) Toll-like receptor 2 mediates proliferation, survival, NF-kappaB translocation, and cytokine mRNA expression in LIF-maintained mouse embryonic stem cells. Stem Cells Dev. 19, 1333-1341
22. Tye, H., Kennedy, C. L., Najdovska, M., McLeod, L., McCormack, W., Hughes, N., Dev, A., Sievert, W., Ooi, C. H., Ishikawa, T. O., Oshima, H., Bhathal, P. S., Parker, A. E., Oshima, M., Tan, P., and Jenkins, B. J. (2012) STAT3-Driven upregulation of TLR2 promotes gastric tumorigenesis independent of tumor inflammation. Cancer Cell 22, 466-478
23. Xie, W., Wang, Y., Huang, Y., Yang, H., Wang, J., and Hu, Z. (2009) Toll-like receptor 2 mediates invasion via activating NF-kappaB in MDA-MB-231 breast cancer cells. Biochem. Biophys. Res. Commun. 379, 1027-1032
24. Kawai, T., and Akira, S. (2007) TLR signaling. Semin. Immunol. 19, 24-32
25. Fan, J. (2010) TLR cross-talk mechanism of hemorrhagic shockprimed pulmonary neutrophil infiltration. Open Crit. Care Med. J. 2, 1-8
26. Chang, Z. L. (2010) Important aspects of Toll-like receptors, ligands and their signaling pathways. Inflamm. Res. 59, 791-808
27. Yang, H., Ochani, M., Li, J., Qiang, X., Tanovic, M., Harris, H. E., Susarla, S. M., Ulloa, L., Wang, H., DiRaimo, R., Czura, C. J., Roth, J., Warren, H. S., Fink, M. P., Fenton, M. J., Andersson, U., and Tracey, K. J. (2004) Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. U. S. A. 101, 296-301
28. Xie, W., Huang, Y., Guo, A., and Wu, W. (2010) Bacteria peptidoglycan promoted breast cancer cell invasiveness and adhesiveness by targeting toll-like receptor 2 in the cancer cells. PLoS One 5, e10850
29. Morrison, R., Schleicher, S. M., Sun, Y., Niermann, K. J., Kim, S., Spratt, D. E., Chung, C. H., and Lu, B. (2011) Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J. Oncol. 2011, 941876
30. Huang, Y., Cai, B., Xu, M., Qiu, Z., Tao, Y., Zhang, Y., Wang, J., Xu, Y., Zhou, Y., Yang, J., Han, X., and Gao, Q. (2012) Gene silencing of toll-like receptor 2 inhibits proliferation of human liver cancer cells and secretion of inflammatory cytokines. PLoS One 7, e38890
31. Yang, H. Z., Cui, B., Liu, H. Z., Mi, S., Yan, J., Yan, H. M., Hua, F., Lin, H., Cai, W. F., Xie, W. J., Lv, X. X., Wang, X. X., Xin, B. M., Zhan, Q. M., and Hu, Z. W. (2009) Blocking TLR2 activity attenuates pulmonary metastases of tumor. PLoS One 4, e6520
32. Kim, S., and Karin, M. (2011) Role of TLR2-dependent inflammation in metastatic progression. Ann. N. Y. Acad. Sci. 1217, 191-206
33. Carotenuto, P., Roma, C., Rachiglio, A. M., Botti, G., D'Alessio, A., and Normanno, N. (2010) Triple negative breast cancer: from molecular portrait to therapeutic intervention. Crit. Rev. Eukaryot. Gene Expr. 20, 17-34
34. Chefetz, I., Alvero, A. B., Holmberg, J. C., Lebowitz, N., Craveiro, V., Yang-Hartwich, Y., Yin, G., Squillace, L., Gurrea Soteras, M., Aldo, P., and Mor, G. (2013) TLR2 enhances ovarian cancer stem cell self-renewal and promotes tumor repair and recurrence. Cell Cycle 12, 511-521
35. Campana, L., Bosurgi, L., and Rovere-Querini, P. (2008) HMGB1: a two-headed signal regulating tumor progression and immunity. Curr. Opin. Immunol. 20, 518-523
36. Nogueira-Machado, J. A., and de Oliveira Volpe, C. M. (2012) HMGB-1 as a target for inflammation controlling. Recent Pat. Endocr. Metab. Immune Drug Discov. 6, 201-209
37. Korkaya, H., Liu, S., and Wicha, M. S. (2011) Regulation of cancer stem cells by cytokine networks: attacking cancer's inflammatory roots. Clin. Cancer Res. 17, 6125-6129
38. Liu, Z., Bandyopadhyay, A., Nichols, R. W., Wang, L., Hinck, A. P., Wang, S., and Sun, L. Z. (2012) Blockade of autocrine TGF-beta signaling inhibits stem cell phenotype, survival, and metastasis of murine breast cancer cells. J. Stem Cell Res. Ther. 2, 1-8
39. Shaykhiev, R., Behr, J., and Bals, R. (2008) Microbial patterns signaling via Toll-like receptors 2 and 5 contribute to epithelial repair, growth and survival. PloS One 3, e1393
40. West, X. Z., Malinin, N. L., Merkulova, A. A., Tischenko, M., Kerr, B. A., Borden, E. C., Podrez, E. A., Salomon, R. G., and Byzova, T. V. (2010) Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature 467, 972-976