Tumor-associated macrophages promote oral cancer progression through activation of the Axl signaling pathway

Annals of Surgical Oncology

Volumn 21, Issue 3, 2014, Pages 1031-1037

  Lee, Chien Hsing ^a   Liu, Shyun Yeu ^b   Chou, Kuo Chou ^a   Yeh, Chi Tai ^c   Shiah, Shine Gwo ^d   Huang, Ren Yeong ^a   Cheng, Jen Chan ^e   Yen, Ching Yu ^b   Shieh, Yi Shing ^a,f  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b CHI MEI MEDICAL CENTER   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e Department of Psychiatry   (Taiwan)

^f NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ARREST SPECIFIC PROTEIN 6; I KAPPA B ALPHA; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; P CADHERIN; PROTEIN ZO1; UVOMORULIN; VIMENTIN;

ARTICLE; CANCER CELL; CANCER TISSUE; CELL INTERACTION; CELL INVASION; CELL MIGRATION; COCULTURE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUTH SQUAMOUS CELL CARCINOMA; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH;

BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; IMMUNOENZYME TECHNIQUES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; MOUTH NEOPLASMS; NF-KAPPA B; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84896694386     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-013-3400-0     Document Type: Article

References (27)

1. Schmidt T, Ben-Batalla I, Schultze A, Loges S. Macrophage-tumor crosstalk: role of TAMR tyrosine kinase receptors and of their ligands. Cell Mol Life Sci. 2012;69:1391-414.
2. Solinas G, Germano G, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol. 2009;86:1065-73.
3. Shieh YS, Hung YJ, Hsieh CB, Chen JS, Chou KC, Liu SY. Tumor-associated macrophage correlated with angiogenesis and progression of mucoepidermoid carcinoma of salivary glands. Ann Surg Oncol. 2009;16:751-60.
4. Kang JC, Chen JS, Lee CH, Chang JJ, Shieh YS. Intratumoral macrophage counts correlate with tumor progression in colorectal cancer. J Surg Oncol. 2010;102:242-8.
5. O'Bryan JP, Frye RA, Cogswell PC, et al. Axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol. 1991;11:5016-31.
6. Schneider C, King RM, Philipson L. Genes specifically expressed at growth arrest of mammalian cells. Cell. 1988;54:787-93.
7. Tjwa M, Bellido-Martin L, Lin Y, et al. Gas6 promotes inflammation by enhancing interactions between endothelial cells, platelets, and leukocytes. Blood. 2008;111:4096-105.
8. Loges S, Schmidt T, Tjwa M, et al. Malignant cells fuel tumor growth by educating infiltrating leukocytes to produce the mitogen Gas6. Blood. 2010;115:2264-73.
9. Sawabu T, Seno H, Kawashima T, et al. Growth arrest-specific gene 6 and Axl signaling enhances gastric cancer cell survival via Akt pathway. Mol Carcinog. 2007;46:155-64.
10. Korshunov VA. Axl-dependent signalling: a clinical update. Clin Sci (Lond). 2012;122:361-8.
11. Sasaki T, Knyazev PG, Clout NJ, et al. Structural basis for Gas6-Axl signalling. EMBO J. 2006;25:80-7.
12. Lee CH, Yen CY, Liu SY, et al. Axl is a prognostic marker in oral squamous cell carcinoma. Ann Surg Oncol. 2012;19(Suppl 3):500-8.
13. Lee CH, Hung HW, Hung PH, Shieh YS. Epidermal growth factor receptor regulates beta-catenin location, stability, and transcriptional activity in oral cancer. Mol Cancer. 2010;9:64.
14. Liu SY, Chang LC, Pan LF, et al. Clinicopathologic significance of tumor cell-lined vessel and microenvironment in oral squamous cell carcinoma. Oral Oncol. 2008;44:277-85.
15. Huang Y, Snuderl M, Jain RK. Polarization of tumor-associated macrophages: a novel strategy for vascular normalization and antitumor immunity. Cancer Cell. 2011;19:1-2.
16. Wang HW, Joyce JA. Alternative activation of tumor-associated macrophages by IL-4: priming for protumoral functions. Cell Cycle. 2010;9:4824-35.
17. Linger RM, Keating AK, Earp HS, Graham DK. Taking aim at Mer and Axl receptor tyrosine kinases as novel therapeutic targets in solid tumors. Expert Opin Ther Targets. 2010;14:1073-90.
18. Sainaghi PP, Castello L, Bergamasco L, Galletti M, Bellosta P, Avanzi GC. Gas6 induces proliferation in prostate carcinoma cell lines expressing the Axl receptor. J Cell Physiol. 2005;204:36-44.
19. Hutterer M, Knyazev P, Abate A, et al. Axl and growth arrest-specific gene 6 are frequently overexpressed in human gliomas and predict poor prognosis in patients with glioblastoma multiforme. Clin Cancer Res. 2008;14:130-8.
20. Fernandez-Fernandez L, Bellido-Martin L, Garcia de Frutos P. Growth arrest-specific gene 6 (GAS6). An outline of its role in haemostasis and inflammation. Thromb Haemost. 2008;100:604-10.
21. Lafdil F, Chobert MN, Couchie D, Brouillet A, Zafrani ES, Mavier P, Laperche Y. Induction of Gas6 protein in CCl4-induced rat liver injury and anti-apoptotic effect on hepatic stellate cells. Hepatology. 2006;44:228-39.
22. Demarchi F, Verardo R, Varnum B, Brancolini C, Schneider C. Gas6 anti-apoptotic signaling requires NF-kappa B activation. J Biol Chem. 2001;276:31738-44.
23. Tai KY, Shieh YS, Lee CS, Shiah SG, Wu CW. Axl promotes cell invasion by inducing MMP-9 activity through activation of NF-kappaB and Brg-1. Oncogene. 2008;27:4044-55.
24. Shankar SL, O'Guin K, Cammer M, et al. The growth arrest-specific gene product Gas6 promotes the survival of human oligodendrocytes via a phosphatidylinositol 3-kinase-dependent pathway. J Neurosci. 2003;23:4208-18.
25. Shankar SL, O'Guin K, Kim M, et al. Gas6/Axl signaling activates the phosphatidylinositol 3-kinase/Akt1 survival pathway to protect oligodendrocytes from tumor necrosis factor alpha-induced apoptosis. J Neurosci. 2006;26:5638-48.
26. Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 1999;401:86-90.
27. Hagemann T, Wilson J, Kulbe H, et al. Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. J Immunol. 2005;175:1197-205.