Novel role of ASC as a regulator of metastatic phenotype

Cancer Medicine

Volumn 5, Issue 9, 2016, Pages 2487-2500

  Okada, Nagisa ^a,b   Fujii, Chifumi ^a,c   Matsumura, Tomio ^a   Kitazawa, Masato ^a,b   Okuyama, Ryuhei ^b   Taniguchi, Shun'ichiro ^a,b,c   Hida, Shigeaki ^d  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c SHINSHU UNIVERSITY   (Japan)

^d NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

ASC; invadopodia; metastasis; motility; Src signaling pathway

Indexed keywords

ADAPTOR PROTEIN; APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN CONTAINING A CASPASE RECRUITMENT DOMAIN; CASPASE 8; PROTEIN TYROSINE KINASE; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B16BL6 CELL LINE; CANCER GROWTH; CANCER MODEL; CELL MIGRATION ASSAY; CELL MOTILITY; CONTROLLED STUDY; CYTOSKELETON; ENZYME PHOSPHORYLATION; GENE SILENCING; GENETIC TRANSDUCTION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MELANOMA B16; MELANOMA CELL LINE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PODOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; SCRATCH ASSAY; SIGNAL TRANSDUCTION; TUMOR INVASION;

EID: 84991056211     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.800     Document Type: Article

References (48)

1. Masumoto, J., S. Taniguchi, K. Ayukawa, H. Sarvotham, T. Kishino, N. Niikawa, et al. 1999. ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J. Biol. Chem. 274:33835–33838.
2. Taniguchi, S., and J. Sagara. 2007. Regulatory molecules involved in inflammasome formation with special reference to a key mediator protein, ASC. Semin. Immunopathol. 29:231–238.
3. Schroder, K., and J. Tschopp. 2010. The inflammasomes. Cell 140:821–832.
4. Rathinam, V. A., S. K. Vanaja, and K. A. Fitzgerald. 2012. Regulation of inflammasome signaling. Nat. Immunol. 13:333–342.
5. Conway, K. E., B. B. McConnell, C. E. Bowring, C. D. Donald, S. T. Warren, and P. M. Vertino. 2000. TMS1, a novel proapoptotic caspase recruitment domain protein, is a target of methylation-induced gene silencing in human breast cancers. Cancer Res. 60:6236–6242.
6. Salminen, A., A. Kauppinen, M. Hiltunen, and K. Kaarniranta. 2014. Epigenetic regulation of ASC/TMS1 expression: potential role in apoptosis and inflammasome function. Cell. Mol. Life Sci. 71:1855–1864.
7. Guan, X., J. Sagara, T. Yokoyama, Y. Koganehira, M. Oguchi, T. Saida, et al. 2003. ASC/TMS1, a caspase-1 activating adaptor, is downregulated by aberrant methylation in human melanoma. Int. J. Cancer 107:202–208.
8. Yokoyama, T., J. Sagara, X. Guan, J. Masumoto, M. Takeoka, Y. Komiyama, et al. 2003. Methylation of ASC/TMS1, a proapoptotic gene responsible for activating procaspase-1, in human colorectal cancer. Cancer Lett. 202:101–108.
9. Machida, E. O., M. V. Brock, C. M. Hooker, J. Nakayama, A. Ishida, J. Amano, et al. 2006. Hypermethylation of ASC/TMS1 is a sputum marker for late-stage lung cancer. Cancer Res. 66:6210–6218.
10. Shimane, T., H. Kobayashi, M. Takeoka, M. Kitazawa, T. Matsumura, S. Hida, et al. 2013. Clinical significance of apoptosis-associated speck-like protein containing a caspase recruitment domain in oral squamous cell carcinoma. Oral. Surg. Oral. Med. Oral. Pathol. Oral. Radiol. 115:799–809.
11. Collard, R. L., N. S. Harya, F. A. Monzon, C. E. Maier, and D. S. O'Keefe. 2006. Methylation of the ASC gene promoter is associated with aggressive prostate cancer. Prostate 66:687–695.
12. Das, P. M., K. Ramachandran, J. Vanwert, L. Ferdinand, G. Gopisetty, I. M. Reis, et al. 2006. Methylation mediated silencing of TMS1/ASC gene in prostate cancer. Mol. Cancer. 5:28.
13. Martinez, R., G. Schackert, and M. Esteller. 2007. Hypermethylation of the proapoptotic gene TMS1/ASC: prognostic importance in glioblastoma multiforme. J. Neurooncol. 82:133–139.
14. Zhang, C., H. Li, G. Zhou, Q. Zhang, T. Zhang, J. Li, et al. 2007. Transcriptional silencing of the TMS1/ASC tumour suppressor gene by an epigenetic mechanism in hepatocellular carcinoma cells. J. Pathol. 212:134–142.
15. Kordi Tamandani, D. M., R. C. Sobti, M. Shekari, and A. Huria. 2009. CpG island methylation of TMS1/ASC and CASP8 genes in cervical cancer. Eur. J. Med. Res. 14:71–75.
16. Liu, Q., J. Jin, J. Ying, Y. Cui, M. Sun, L. Zhang, et al. 2015. Epigenetic inactivation of the candidate tumor suppressor gene ASC/TMS1 in human renal cell carcinoma and its role as a potential therapeutic target. Oncotarget 6:22706–22723.
17. Wu, L., C. Zhang, X. Wang, X. Ding, J. Deng, and H. Liang. 2016. Methylation of ASC/TMS1 promoter is associated with poor prognosis of patients with gastric cancer. Clin. Transl. Oncol. 18:296–303.
18. Yamamoto, M., K. Yaginuma, H. Tsutsui, J. Sagara, X. Guan, E. Seki, et al. 2004. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules. Genes Cells 9:1055–1067.
19. Poste, G., J. Doll, I. R. Hart, and I. J. Fidler. 1980. In vitro selection of murine B16 melanoma variants with enhanced tissue-invasive properties. Cancer Res. 40:1636–1644.
20. Margadant, C., K. Raymond, M. Kreft, N. Sachs, H. Janssen, and A. Sonnenberg. 2009. Integrin alpha3beta1 inhibits directional migration and wound re-epithelialization in the skin. J. Cell Sci. 122:278–288.
21. Thiery, J. P. 2002. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2:442–454.
22. Chen, W. T. 1989. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 251:167–185.
23. Weaver, A. M. 2006. Invadopodia: specialized cell structures for cancer invasion. Clin. Exp. Metastasis 23:97–105.
24. Poincloux, R., F. Lizarraga, and P. Chavrier. 2009. Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122:3015–3024.
25. Carman, C. V. 2009. Mechanisms for transcellular diapedesis: probing and pathfinding by ‘invadosome-like protrusions’. J. Cell Sci. 122:3025–3035.
26. Albiges-Rizo, C., O. Destaing, B. Fourcade, E. Planus, and M. R. Block. 2009. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 122:3037–3049.
27. Linder, S. 2009. Invadosomes at a glance. J. Cell Sci. 122:3009–3013.
28. Guarino, M. 2010. Src signaling in cancer invasion. J. Cell. Physiol. 223:14–26.
29. Tague, S. E., V. Muralidharan, and C. D'Souza-Schorey. 2004. ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc. Natl Acad. Sci. USA 101:9671–9676.
30. Frisch, S. M. 2008. Caspase-8: fly or die. Cancer Res. 68:4491–4493.
31. Graf, R. P., N. Keller, S. Barbero, and D. Stupack. 2014. Caspase-8 as a regulator of tumor cell motility. Curr. Mol. Med. 14:246–254.
32. Barbero, S., D. Barila, A. Mielgo, V. Stagni, K. Clair, and D. Stupack. 2008. Identification of a critical tyrosine residue in caspase 8 that promotes cell migration. J. Biol. Chem. 283:13031–13034.
33. Masumoto, J., T. A. Dowds, P. Schaner, F. F. Chen, Y. Ogura, M. Li, et al. 2003. ASC is an activating adaptor for NF-kappa B and caspase-8-dependent apoptosis. Biochem. Biophys. Res. Commun. 303:69–73.
34. Vajjhala, P. R., A. Lu, D. L. Brown, S. W. Pang, V. Sagulenko, D. P. Sester, et al. 2015. The inflammasome adaptor ASC induces procaspase-8 death effector domain filaments. J. Biol. Chem. 290:29217–29230.
35. Sen, B., and F. M. Johnson. 2011. Regulation of SRC family kinases in human cancers. J. Signal. Transduct. 2011:865819.
36. Peinado, H., M. Aleckovic, S. Lavotshkin, I. Matei, B. Costa-Silva, G. Moreno-Bueno, et al. 2012. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18:883–891.
37. Trusolino, L., A. Bertotti, and P. M. Comoglio. 2010. MET signalling: principles and functions in development, organ regeneration and cancer. Nat. Rev. Mol. Cell Biol. 11:834–848.
38. Zhu, S., J. D. Bjorge, and D. J. Fujita. 2007. PTP1B contributes to the oncogenic properties of colon cancer cells through Src activation. Cancer Res. 67:10129–10137.
39. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, et al. 2000. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 404:999–1003.
40. Giannoni, E., F. Buricchi, G. Raugei, G. Ramponi, and P. Chiarugi. 2005. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell. Biol. 25:6391–6403.
41. Sakurai-Yageta, M., C. Recchi, G. Le Dez, J. B. Sibarita, L. Daviet, J. Camonis, et al. 2008. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181:985–998.
42. Roy, M., Z. Li, and D. B. Sacks. 2005. IQGAP1 is a scaffold for mitogen-activated protein kinase signaling. Mol. Cell. Biol. 25:7940–7952.
43. Waite, A. L., P. Schaner, C. Hu, N. Richards, B. Balci-Peynircioglu, A. Hong, et al. 2009. Pyrin and ASC co-localize to cellular sites that are rich in polymerizing actin. Exp. Biol. Med. (Maywood) 234:40–52.
44. Liu, W., Y. Luo, J. H. Dunn, D. A. Norris, C. A. Dinarello, and M. Fujita. 2013. Dual role of apoptosis-associated speck-like protein containing a CARD (ASC) in tumorigenesis of human melanoma. J. Invest. Dermatol. 133:518–527.
45. Orosz, P., B. Echtenacher, W. Falk, J. Ruschoff, D. Weber, and D. N. Mannel. 1993. Enhancement of experimental metastasis by tumor necrosis factor. J. Exp. Med. 177:1391–1398.
46. Orosz, P., A. Kruger, M. Hubbe, J. Ruschoff, P. Von Hoegen, and D. N. Mannel. 1995. Promotion of experimental liver metastasis by tumor necrosis factor. Int. J. Cancer 60:867–871.
47. Finlay, D., and K. Vuori. 2007. Novel noncatalytic role for caspase-8 in promoting SRC-mediated adhesion and Erk signaling in neuroblastoma cells. Cancer Res. 67:11704–11711.
48. Barbero, S., A. Mielgo, V. Torres, T. Teitz, D. J. Shields, D. Mikolon, et al. 2009. Caspase-8 association with the focal adhesion complex promotes tumor cell migration and metastasis. Cancer Res. 69:3755–3763.