Receptor activator of NF-κ B ligand induces cell adhesion and integrin α2 expression via NF-κ B in head and neck cancers

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Yamada, Tamaki ^a,b   Tsuda, Masumi ^a   Wagatsuma, Takanori ^a   Fujioka, Yoichiro ^a   Fujioka, Mari ^a   Satoh, Aya O ^a   Horiuchi, Kosui ^a   Nishide, Shinya ^a   Nanbo, Asuka ^a   Totsuka, Yasunori ^b   Haga, Hisashi ^b   Tanaka, Shinya ^a   Shindoh, Masanobu ^b   Ohba, Yusuke ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OSTEOCLAST DIFFERENTIATION FACTOR; TNFSF11 PROTEIN, HUMAN;

ANIMAL; CANCER TRANSPLANTATION; CELL ADHESION; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; HEAD AND NECK TUMOR; HUMAN; METABOLISM; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; INTEGRIN ALPHA2; MICE; NEOPLASM TRANSPLANTATION; NF-KAPPA B; RANK LIGAND; SIGNAL TRANSDUCTION;

EID: 84962210755     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23545     Document Type: Article

References (67)

1. Reichart, P. A. Identification of risk groups for oral precancer and cancer and preventive measures. Clin Oral Investig 5, 207-213 (2001).
2. Onoue, T. et al. Epithelial-mesenchymal transition induced by the stromal cell-derived factor-1/CXCR4 system in oral squamous cell carcinoma cells. Int J Onco. 29, 1133-1138 (2006).
3. Chang, J. Y. F., Wright, J. M. & Svoboda, K. K. H. Signal transduction pathways involved in epithelial-mesenchymal transition in oral cancer compared with other cancers. Cells Tissues Organs (Print) 185, 40-47 (2007).
4. Tsuda, M. & Ohba, Y. Functional Biomarkers of Oral Cancer. 277-294 (InTech, 2012).
5. Giancotti, F. & Ruoslahti, E. Integrin signaling. Science 285, 1028-1032 (1999).
6. Pilewski, J. M., Latoche, J. D., Arcasoy, S. M. & Albelda, S. M. Expression of integrin cell adhesion receptors during human airway epithelial repair in vivo. Am J Physiol 273, L256-63 (1997).
7. Mizejewski, G. J. Role of integrins in cancer: Survey of expression patterns. Proc Soc Exp Biol Med 222, 124-138 (1999).
8. Alexandrova, A. Y. Evolution of cell interactions with extracellular matrix during carcinogenesis. Biochem Mosc 73, 733-741 (2008).
9. Avnur, Z. & Geiger, B. The removal of extracellular fibronectin from areas of cell-substrate contact. Cell 25, 121-132 (1981).
10. Tamkun, J. W. et al. Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell 46, 271-282 (1986).
11. Park, C. C. et al. β 1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 66, 1526-1535 (2006).
12. Grzesiak, J. J. & Bouvet, M. The α2β1 1 integrin mediates the malignant phenotype on type I collagen in pancreatic cancer cell lines. Br J Cancer 94, 1311-1319 (2006).
13. Böttger, T. C. et al. Prognostic value of immunohistochemical expression of β-1 integrin in pancreatic carcinoma. Oncology 56, 308-313 (1999).
14. Thomas, G. J., Jones, J. & Speight, P. M. Integrins and oral cancer. Oral Oncol 33, 381-388 (1997).
15. Bagutti, C., Speight, P. M. & Watt, F. M. Comparison of integrin, cadherin, and catenin expression in squamous cell carcinomas of the oral cavity. J Pathol 186, 8-16 (1998).
16. Yamamura, K., Kibbey, M. C. & Kleinman, H. K. Melanoma cells selected for adhesion to laminin peptides have different malignant properties. Cancer Res 53, 423-428 (1993).
17. Kanemoto, T. et al. Identification of an amino acid sequence from the laminin A chain that stimulates metastasis and collagenase IV production. Proc Natl Acad Sci USA 87, 2279-2283 (1990).
18. Yamada, T. et al. RANKL Expression Specifically Observed in Vivo Promotes Epithelial Mesenchymal Transition and Tumor Progression. Am J Pathol 178, 2845-2856 (2011).
19. Cardone, M., Salvesen, G., Widmann, C., Johnson, G. & Frisch, S. The regulation of anoikis: MEKK-1 activation requires cleavage by caspases. Cell 90, 315-323 (1997).
20. Hynes, R. Integrins: Bidirectional, allosteric signaling machines. Cell 110, 673-687 (2002).
21. Takada, Y., Ye, X. & Simon, S. The integrins. Genome Biol 8, 215 (2007).
22. Sokoloski, J. A., Sartorelli, A. C., Rosen, C. A. & Narayanan, R. Antisense oligonucleotides to the p65 subunit of NF-κ B block CD11b expression and alter adhesion properties of differentiated HL-60 granulocytes. Blood 82, 625-632 (1993).
23. Qwarnström, E. E., Ostberg, C. O., Turk, G. L., Richardson, C. A. & Bomsztyk, K. Fibronectin attachment activates the NF-κ B p50/p65 heterodimer in fibroblasts and smooth muscle cells. J Biol Chem 269, 30765-30768 (1994).
24. Narayanan, R., Higgins, K. A., Perez, J. R., Coleman, T. A. & Rosen, C. A. Evidence for differential functions of the p50 and p65 subunits of NF-κ B with a cell adhesion model. Mol Cell Biol 13, 3802-3810 (1993).
25. Lin, T. H. et al. Integrin-mediated tyrosine phosphorylation and cytokine message induction in monocytic cells. A possible signaling role for the Syk tyrosine kinase. J Biol Chem 270, 16189-16197 (1995).
26. Feaver, R. E., Hastings, N. E., Pryor, A. & Blackman, B. R. GRP78 upregulation by atheroprone shear stress via p38-, α 2β 1-dependent mechanism in endothelial cells. Arterioscler Thromb Vasc Biol 28, 1534-1541 (2008).
27. Shaik, S. S. et al. Low intensity shear stress increases endothelial ELR + CXC chemokine production via a focal adhesion kinasep38β MAPK-NF-κ B pathway. J Biol Chem 284, 5945-5955 (2009).
28. Jones, D. H. et al. Regulation of cancer cell migration and bone metastasis by RANKL. Nature 440, 692-696 (2006).
29. Armstrong, A. P. et al. RANKL acts directly on RANK-expressing prostate tumor cells and mediates migration and expression of tumor metastasis genes. Prostate 68, 92-104 (2008).
30. Sezer, O., Heider, U., Zavrski, I., Kühne, C. A. & Hofbauer, L. C. RANK ligand and osteoprotegerin in myeloma bone disease. Blood 101, 2094-2098 (2003).
31. Pearse, R. N. et al. Multiple myeloma disrupts the TRANCE/osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proc Natl Acad Sci USA 98, 11581-11586 (2001).
32. Giuliani, N. et al. Human myeloma cells stimulate the receptor activator of nuclear factor-κ B ligand (RANKL) in T lymphocytes: A potential role in multiple myeloma bone disease. Blood 100, 4615-4621 (2002).
33. Giuliani, N., Bataille, R., Mancini, C., Lazzaretti, M. & Barillé, S. Myeloma cells induce imbalance in the osteoprotegerin/osteoprotegerin ligand system in the human bone marrow environment. Blood 98, 3527-3533 (2001).
34. Caswell, P. T., Vadrevu, S. & Norman, J. C. Integrins: Masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10, 843-853 (2009).
35. Caswell, P. & Norman, J. Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18, 257-263 (2008).
36. Benedetto, S. et al. Quantification of the expression level of integrin receptor α vβ 3 in cell lines and MR imaging with antibodycoated iron oxide particles. Magn Reson Med 56, 711-716 (2006).
37. Shintani, Y., Wheelock, M. J. & Johnson, K. R. Phosphoinositide-3 kinase-Rac1-c-Jun NH2-terminal kinase signaling mediates collagen I-induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol Biol Cell 17, 2963-2975 (2006).
38. Karin, M. Nuclear factor-κ B in cancer development and progression. Nature 441, 431-436 (2006).
39. Baldwin, A. S. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κ B. J Clin Invest 107, 241-246 (2001).
40. Friedl, P. & Wolf, K. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 3, 362-374 (2003).
41. Mori, K. et al. Human osteosarcoma cells express functional receptor activator of nuclear factor-κ B. J Patho. 211, 555-562 (2007).
42. Mori, K. et al. DU145 human prostate cancer cells express functional receptor activator of NFκ B: New insights in the prostate cancer bone metastasis process. Bone 40, 981-990 (2007).
43. Mori, K. et al. Receptor activator of nuclear factor-κ B ligand (RANKL) directly modulates the gene expression profile of RANKpositive Saos-2 human osteosarcoma cells. Oncol Rep 18, 1365-1371 (2007).
44. Wittrant, Y. et al. RANKL directly induces bone morphogenetic protein-2 expression in RANK-expressing POS-1 osteosarcoma cells. Int J Oncol 28, 261-269 (2006).
45. Horwood, N. J., Elliott, J., Martin, T. J. & Gillespie, M. T. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 139, 4743-4746 (1998).
46. Yamada, T. et al. PTHrP promotes malignancy of human oral cancer cell downstream of the EGFR signaling. Biochem Biophys Res Commun 368, 575-581 (2008).
47. Takayanagi, H. et al. RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-? . Nature 416, 744-749 (2002).
48. Liu, W. et al. Functional identification of three receptor activator of NF-? B cytoplasmic motifs mediating osteoclast differentiation and function. J Biol Chem 279, 54759-54769 (2004).
49. Feng, X. Regulatory roles and molecular signaling of TNF family members in osteoclasts. Gene 350, 1-13 (2005).
50. Chung, J. Y., Park, Y. C., Ye, H. & Wu, H. All TRAFs are not created equal: Common and distinct molecular mechanisms of TRAFmediated signal transduction. J Cell Sci 115, 679-688 (2002).
51. Boyle, W. J., Simonet, W. S. & Lacey, D. L. Osteoclast differentiation and activation. Nature 423, 337-342 (2003).
52. Zutter, M. M., Santoro, S. A., Painter, A. S., Tsung, Y. L. & Gafford, A. The human α 2 integrin gene promoter. Identification of positive and negative regulatory elements important for cell-type and developmentally restricted gene expression. J Biol Chem 269, 463-469 (1994).
53. Nissinen, L., Westermarck, J., Koivisto, L., Kähäri, V. M. & Heino, J. Transcription ofα 2 integrin gene in osteosarcoma cells is enhanced by tumor promoters. Exp Cell Res 243, 1-10 (1998).
54. Dingemans, A.-M. C. et al. Integrin expression profiling identifies integrin α 5 andβ 1 as prognostic factors in early stage non-small cell lung cancer. Mol Cancer 9, 152 (2010).
55. Kurokawa, A. et al. Diagnostic value of integrinα 3, β 4, and γ 5 gene expression levels for the clinical outcome of tongue squamous cell carcinoma. Cancer 112, 1272-1281 (2008).
56. Pérez-Martínez, F. C. et al. Receptor activator of nuclear factor-κ B ligand (RANKL) as a novel prognostic marker in prostate carcinoma. Histol Histopathol 23, 709-715 (2008).
57. Lee, S. H. et al. Core3 O-glycan synthase suppresses tumor formation and metastasis of prostate carcinoma PC3 and LNCaP cells through down-regulation of α 2β 1 integrin complex. J Biol Chem 284, 17157-17169 (2009).
58. Ivanova, I. A. et al. FER kinase promotes breast cancer metastasis by regulating α 6-and β 1-integrin-dependent cell adhesion and anoikis resistance. Oncogene 32, 5582-5592 (2013).
59. Carduner, L. et al. Cell cycle arrest or survival signaling through ? v integrins, activation of PKC and ERK1/2 lead to anoikis resistance of ovarian cancer spheroids. Exp Cell Res 320, 329-342 (2014).
60. Silginer, M., Weller, M., Ziegler, U. & Roth, P. Integrin inhibition promotes atypical anoikis in glioma cells. Cell Death Dis 5, e1012 (2014).
61. Morozevich, G. E., Kozlova, N. I., Susova, O. Y., Karalkin, P. A. & Berman, A. E. Implication of α 2β 1 integrin in anoikis of MCF-7 human breast carcinoma cells. Biochem Mosc. 80, 97-103 (2015).
62. Hsieh, Y.-H., Van Der Heyde, H., Oh, E.-S., Guan, J.-L. & Chang, P.-L. Osteopontin mediates tumorigenic transformation of a preneoplastic murine cell line by suppressing anoikis: An Arg-Gly-Asp-dependent-focal adhesion kinase-caspase-8 axis. Mol Carcinog 54, 379-392 (2015).
63. Aslan, B. et al. The ZNF304-integrin axis protects against anoikis in cancer. Nat Commun 6, 7351 (2015).
64. Inuzuka, T. et al. Integral role of transcription factor 8 in the negative regulation of tumor angiogenesis. Cancer Res 69, 1678-1684 (2009).
65. Inuzuka, T., Tsuda, M., Kawaguchi, H. & Ohba, Y. Transcription factor 8 activates R-Ras to regulate angiogenesis. Biochem Biophys Res Commun 379, 510-513 (2009).
66. Fujioka, Y. et al. A Ca(2+)-dependent signalling circuit regulates influenza A virus internalization and infection. Nat Commun 4, 2763 (2013).
67. Montesano, R., Schaller, G. & Orci, L. Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697-711 (1991).