Expression of TLR9 in tumor-infiltrating mononuclear cells enhances angiogenesis and is associated with a worse survival in lung cancer

International Journal of Cancer

Volumn 134, Issue 4, 2014, Pages 765-777

  Belmont, Laure ^a,b   Rabbe, Nathalie ^a,b   Antoine, Martine ^a,b   Cathelin, Dominique ^c   Guignabert, Christophe ^d   Kurie, Jonathan ^e   Cadranel, Jacques ^a,b   Wislez, Marie ^a,b  

^a HÔPITAL TENON   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^e UNIVERSITY OF TEXAS   (United States)

Author keywords

angiogenesis; non small cell lung cancer; prognosis; TLR9 activation

Indexed keywords

TOLL LIKE RECEPTOR 9; VASCULOTROPIN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER STAGING; CANCER SURVIVAL; CAPILLARY DENSITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EARLY CANCER; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCHEMISTRY; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MONONUCLEAR CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; ONCOGENE K RAS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VASCULARIZATION; TUMOR VOLUME;

EID: 84890125832     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28413     Document Type: Article

References (38)

1. Igney FH, Krammer PH,. Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 2002; 71: 907-20.
2. Rakoff-Nahoum S, Medzhitov R,. Toll-like receptors and cancer. Nat Rev Cancer 2009; 9: 57-63.
3. Akira S, Uematsu S, Takeuchi O,. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
4. Iwasaki A, Medzhitov R,. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004; 5: 987-95.
5. Krieg AM,. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002; 20: 709-60.
6. Topalian SL, Weiner GJ, Pardoll DM,. Cancer immunotherapy comes of age. J Clin Oncol 2011; 29: 4828-36.
7. Chen JJW, Lin Y-C, Yao P-L, et al. Tumor-associated macrophages: the double-edged sword in cancer progression. J Clin Oncol 2005; 23: 953-64.
8. Chen JJW, Yao P-L, Yuan A, et al. Up-regulation of tumor interleukin-8 expression by infiltrating macrophages: its correlation with tumor angiogenesis and patient survival in non-small cell lung cancer. Clin Cancer Res 2003; 9: 729-37.
9. Gong Y, Koh D-R,. Neutrophils promote inflammatory angiogenesis via release of preformed VEGF in an in vivo corneal model. Cell Tissue Res 2010; 339: 437-48.
10. Wislez M, Massiani M-A, Milleron B, et al. Clinical characteristics of pneumonic-type adenocarcinoma of the lung. Chest 2003; 123: 1868-77.
11. Wislez M, Rabbe N, Marchal J, et al. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death. Cancer Res 2003; 63: 1405-12.
12. Wislez M, Fleury-Feith J, Rabbe N, et al. Tumor-derived granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor prolong the survival of neutrophils infiltrating bronchoalveolar subtype pulmonary adenocarcinoma. Am J Pathol 2001; 159: 1423-33.
13. Takanami I, Takeuchi K, Naruke M,. Mast cell density is associated with angiogenesis and poor prognosis in pulmonary adenocarcinoma. Cancer 2000; 88: 2686-92.
14. Manegold C, Gravenor D, Woytowitz D, et al. Randomized phase II trial of a toll-like receptor 9 agonist oligodeoxynucleotide, PF-3512676, in combination with first-line taxane plus platinum chemotherapy for advanced-stage non-small-cell lung cancer. J Clin Oncol 2008; 26: 3979-86.
15. Hirsh V, Paz-Ares L, Boyer M, et al. Randomized phase III trial of paclitaxel/carboplatin with or without PF-3512676 (Toll-like receptor 9 agonist) as first-line treatment for advanced non-small-cell lung cancer. J Clin Oncol 2011; 29: 2667-74.
16. Johnson L, Mercer K, Greenbaum D, et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001; 410: 1111-16.
17. Mountain CF,. Revisions in the International System for Staging Lung Cancer. Chest 1997; 111: 1710-17.
18. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408: 740-5.
19. Wislez M, Spencer ML, Izzo JG, et al. Inhibition of mammalian target of rapamycin reverses alveolar epithelial neoplasia induced by oncogenic K-ras. Cancer Res 2005; 65: 3226-35.
20. Bedoret D, Wallemacq H, Marichal T, et al. Lung interstitial macrophages alter dendritic cell functions to prevent airway allergy in mice. J Clin Invest 2009; 119: 3723-38.
21. Zaynagetdinov R, Sherrill TP, Kendall PL, et al. Identification of myeloid cell subsets in murine lungs using flow cytometry. Am J Respir Cell Mol Biol 2013; 49: 180-9.
22. Adams S,. Toll-like receptor agonists in cancer therapy. Immunotherapy 2009; 1: 949-64.
23. Wislez M, Fujimoto N, Izzo JG, et al. High expression of ligands for chemokine receptor CXCR2 in alveolar epithelial neoplasia induced by oncogenic kras. Cancer Res 2006; 66: 4198-207.
24. Kisley LR, Barrett BS, Bauer AK, et al. Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res 2002; 62: 6850-6.
25. Ridnour LA, Cheng RYS, Switzer CH, et al. Molecular pathways: toll-like receptors in the tumor microenvironment-poor prognosis or new therapeutic opportunity. Clin Cancer Res 2013; 19: 1340-6.
26. Cheah MS, Wallace CD, Hoffman RM,. Hypomethylation of DNA in human cancer cells: a site-specific change in the c-myc oncogene. J Natl Cancer Inst 1984; 73: 1057-65.
27. Ehrlich M,. DNA hypomethylation in cancer cells. Epigenomics 2009; 1: 239-59.
28. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006; 355: 2542-50.
29. Reck M, Von Pawel J, Zatloukal P, et al. Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol 2009; 27: 1227-34.
30. Zheng M, Klinman DM, Gierynska M, et al. DNA containing CpG motifs induces angiogenesis. Proc Natl Acad Sci USA 2002; 99: 8944-9.
31. Pinhal-Enfield G, Ramanathan M, Hasko G, et al. An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am J Pathol 2003; 163: 711-21.
32. Chang Y-J, Wu M-S, Lin J-T, et al. Helicobacter pylori-induced invasion and angiogenesis of gastric cells is mediated by cyclooxygenase-2 induction through TLR2/TLR9 and promoter regulation. J Immunol 2005; 175: 8242-52.
33. Ghosh TK, Mickelson DJ, Fink J, et al. Toll-like receptor (TLR) 2-9 agonists-induced cytokines and chemokines. I. Comparison with T cell receptor-induced responses. Cell Immunol 2006; 243: 48-57.
34. Zhang Y-B, He F-L, Fang M, et al. Increased expression of Toll-like receptors 4 and 9 in human lung cancer. Mol Biol Rep 2009; 36: 1475-81.
35. Droemann D, Albrecht D, Gerdes J, et al. Human lung cancer cells express functionally active Toll-like receptor 9. Respir Res 2005; 6: 1.
36. Ren T, Xu L, Jiao S, et al. TLR9 signaling promotes tumor progression of human lung cancer cell in vivo. Pathol Oncol Res 2009; 15: 623-30.
37. Berger R, Fiegl H, Goebel G, et al. Toll-like receptor 9 expression in breast and ovarian cancer is associated with poorly differentiated tumors. Cancer Sci 2010; 101: 1059-66.
38. Cherfils-Vicini J, Platonova S, Gillard M, et al. Triggering of TLR7 and TLR8 expressed by human lung cancer cells induces cell survival and chemoresistance. J Clin Invest 2010; 120: 1285-97.