The ubiquitin-like modifier FAT10 decorates autophagy-targeted Salmonella and contributes to Salmonella resistance in mice

Journal of Cell Science

Volumn 127, Issue 22, 2014, Pages 4883-4893

  Spinnenhirn, Valentina ^a   Farhan, Hesso ^b,c   Basler, Michael ^a,c   Aichem, Annette ^c   Canaan, Allon ^d   Groettrup, Marcus ^a,c  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF KONSTANZ   (Switzerland)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; FAT10; P62; Salmonella Typhimurium; Ubiquitin; Xenophagy

Indexed keywords

ADAPTOR PROTEIN; FAT10 PROTEIN; GAMMA INTERFERON; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; NDP62 PROTEIN; PROTEIN P62; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN; UNCLASSIFIED DRUG; FAT10 PROTEIN, MOUSE; UBD PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BACTERIAL STRAIN; CELL DIVISION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; FEMALE; GENE OVEREXPRESSION; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; KINETICS; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SALMONELLA TYPHIMURIUM; UBIQUITINATION; WILD TYPE; ANIMAL; C57BL MOUSE; HEK293 CELL LINE; METABOLISM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TRANSGENIC MOUSE; UMBILICAL VEIN ENDOTHELIAL CELL;

BACTERIA (MICROORGANISMS); EUKARYOTA; MUS; MUS MUSCULUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

ANIMALS; AUTOPHAGY; HEK293 CELLS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SALMONELLA TYPHIMURIUM; UBIQUITIN; UBIQUITINS;

EID: 84911978547     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.152371     Document Type: Article

References (50)

1. Aichem, A., Pelzer, C., Lukasiak, S., Kalveram, B., Sheppard, P. W., Rani, N., Schmidtke, G. and Groettrup, M. (2010). USE1 is a bispecific conjugating enzyme for ubiquitin and FAT10, which FAT10ylates itself in cis. Nat. Commun. 1, 13.
2. Aichem, A., Kalveram, B., Spinnenhirn, V., Kluge, K., Catone, N., Johansen, T. and Groettrup, M. (2012). The proteomic analysis of endogenous FAT10 substrates identifies p62/SQSTM1 as a substrate of FAT10ylation. J. Cell Sci. 125, 4576-4585.
3. Bates, E. E., Ravel, O., Dieu, M. C., Ho, S., Guret, C., Bridon, J. M., Ait-Yahia, S., Briè re, F., Caux, C., Banchereau, J. et al. (1997). Identification and analysis of a novel member of the ubiquitin family expressed in dendritic cells and mature B cells. Eur. J. Immunol. 27, 2471-2477.
4. Birmingham, C. L., Smith, A. C., Bakowski, M. A., Yoshimori, T. and Brumell, J. H. (2006). Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J. Biol. Chem. 281, 11374-11383.
5. Bjørkøy, G., Lamark, T., Brech, A., Outzen, H., Perander, M., Overvatn, A., Stenmark, H. and Johansen, T. (2005). p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtininduced cell death. J. Cell Biol. 171, 603-614.
6. Canaan, A., Yu, X., Booth, C. J., Lian, J., Lazar, I., Gamfi, S. L., Castille, K., Kohya, N., Nakayama, Y., Liu, Y. C. et al. (2006). FAT10/diubiquitin-like protein-deficient mice exhibit minimal phenotypic differences. Mol. Cell. Biol. 26, 5180-5189.
7. Cemma, M., Kim, P. K. and Brumell, J. H. (2011). The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteriaassociated microdomains to target Salmonella to the autophagy pathway. Autophagy 7, 341-345.
8. Chiu, Y. H., Sun, Q. and Chen, Z. J. (2007). E1-L2 activates both ubiquitin and FAT10. Mol. Cell 27, 1014-1023.
9. Deretic, V. and Levine, B. (2009). Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5, 527-549.
10. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G. T., van der Goot, F. G., Sansonetti, P. J. and Lafont, F. (2009). Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6, 137-149.
11. Fan, W., Cai,W., Parimoo, S., Schwarz, D. C., Lennon, G. G. andWeissman, S. M. (1996). Identification of seven new human MHC class I region genes around the HLA-F locus. Immunogenetics 44, 97-103.
12. Fujita, N., Morita, E., Itoh, T., Tanaka, A., Nakaoka, M., Osada, Y., Umemoto, T., Saitoh, T., Nakatogawa, H., Kobayashi, S. et al. (2013). Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 203, 115-128.
13. Gao, Y., Theng, S. S., Zhuo, J., Teo, W. B., Ren, J. and Lee, C. G. (2014). FAT10, an ubiquitin-like protein, confers malignant properties in non-tumorigenic and tumorigenic cells. Carcinogenesis 35, 923-934.
14. Gong, P., Canaan, A.,Wang, B., Leventhal, J., Snyder, A., Nair, V., Cohen, C. D., Kretzler, M., D'Agati, V., Weissman, S. et al. (2010). The ubiquitin-like protein FAT10 mediates NF-kappaB activation. J. Am. Soc. Nephrol. 21, 316-326.
15. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I. and Deretic, V. (2004). Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766.
16. Hipp, M. S., Raasi, S., Groettrup, M. and Schmidtke, G. (2004). NEDD8 ultimate buster-1L interacts with the ubiquitin-like protein FAT10 and accelerates its degradation. J. Biol. Chem. 279, 16503-16510.
17. Hipp, M. S., Kalveram, B., Raasi, S., Groettrup, M. and Schmidtke, G. (2005). FAT10, a ubiquitin-independent signal for proteasomal degradation. Mol. Cell. Biol. 25, 3483-3491.
18. Huett, A., Heath, R. J., Begun, J., Sassi, S. O., Baxt, L. A., Vyas, J. M., Goldberg, M. B. and Xavier, R. J. (2012). The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium. Cell Host Microbe 12, 778-790.
19. Jiang, X. and Chen, Z. J. (2012). The role of ubiquitylation in immune defence and pathogen evasion. Nat. Rev. Immunol. 12, 35-48.
20. Jin, J., Li, X., Gygi, S. P. and Harper, J. W. (2007). Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447, 1135-1138.
21. Kalveram, B., Schmidtke, G. and Groettrup, M. (2008). The ubiquitin-like modifier FAT10 interacts with HDAC6 and localizes to aggresomes under proteasome inhibition. J. Cell Sci. 121, 4079-4088.
22. Kirkin, V., McEwan, D. G., Novak, I. and Dikic, I. (2009). A role for ubiquitin in selective autophagy. Mol. Cell 34, 259-269.
23. Lee, C. G., Ren, J., Cheong, I. S., Ban, K. H., Ooi, L. L., Yong Tan, S., Kan, A., Nuchprayoon, I., Jin, R., Lee, K. H. et al. (2003). Expression of the FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene 22, 2592-2603.
24. Liu, Y. C., Pan, J., Zhang, C., Fan, W., Collinge, M., Bender, J. R. and Weissman, S. M. (1999). A MHC-encoded ubiquitin-like protein (FAT10) binds noncovalently to the spindle assembly checkpoint protein MAD2. Proc. Natl. Acad. Sci. USA 96, 4313-4318.
25. Lukasiak, S., Schiller, C., Oehlschlaeger, P., Schmidtke, G., Krause, P., Legler, D. F., Autschbach, F., Schirmacher, P., Breuhahn, K. and Groettrup, M. (2008). Proinflammatory cytokines cause FAT10 upregulation in cancers of liver and colon. Oncogene 27, 6068-6074.
26. Merbl, Y., Refour, P., Patel, H., Springer, M. and Kirschner, M. W. (2013). Profiling of ubiquitin-like modifications reveals features of mitotic control. Cell 152, 1160-1172.
27. Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K. et al. (2004). Autophagy defends cells against invading group A Streptococcus. Science 306, 1037-1040.
28. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N. and Sasakawa, C. (2005). Escape of intracellular Shigella from autophagy. Science 307, 727-731.
29. Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G. and Johansen, T. (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145.
30. Pelzer, C., Kassner, I., Matentzoglu, K., Singh, R. K., Wollscheid, H. P., Scheffner, M., Schmidtke, G. and Groettrup, M. (2007). UBE1L2, a novel E1 enzyme specific for ubiquitin. J. Biol. Chem. 282, 23010-23014.
31. Perrin, A. J., Jiang, X., Birmingham, C. L., So, N. S. Y. and Brumell, J. H. (2004). Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr. Biol. 14, 806-811.
32. Ponpuak, M., Davis, A. S., Roberts, E. A., Delgado, M. A., Dinkins, C., Zhao, Z., Virgin, H. W., IV, Kyei, G B., Johansen, T., Vergne, I, et al. (2010). Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 32, 329-341.
33. Raasi, S., Schmidtke, G., de Giuli, R. and Groettrup, M. (1999). A ubiquitin-like protein which is synergistically inducible by interferon-c and tumor necrosis factor-a. Eur. J. Immunol. 29, 4030-4036.
34. Raasi, S., Schmidtke, G. and Groettrup, M. (2001). The ubiquitin-like protein FAT10 forms covalent conjugates and induces apoptosis. J. Biol. Chem. 276, 35334-35343.
35. Rani, N., Aichem, A., Schmidtke, G., Kreft, S. G. and Groettrup, M. (2012). FAT10 and NUB1L bind to the VWA domain of Rpn10 and Rpn1 to enable proteasome-mediated proteolysis. Nat. Commun. 3, 749-749.
36. Ren, J., Wang, Y., Gao, Y., Mehta, S. B. K. and Lee, C. G. L. (2011). FAT10 mediates the effect of TNF-a in inducing chromosomal instability. J. Cell Sci. 124, 3665-3675.
37. Ross, M. J., Wosnitzer, M. S., Ross, M. D., Granelli, B., Gusella, G. L., Husain, M., Kaufman, L., Vasievich, M., D'Agati, V. D., Wilson, P. D. et al. (2006). Role of ubiquitin-like protein FAT10 in epithelial apoptosis in renal disease. J. Am. Soc. Nephrol. 17, 996-1004.
38. Schmidtke, G., Kalveram, B. and Groettrup, M. (2009). Degradation of FAT10 by the 26S proteasome is independent of ubiquitylation but relies on NUB1L. FEBS Lett. 583, 591-594.
39. Schmidtke, G., Aichem, A. and Groettrup, M. (2014). FAT10ylation as a signal for proteasomal degradation. Biochim. Biophys. Acta 1843, 97-102.
40. Schwan, W. R., Huang, X. Z., Hu, L. and Kopecko, D. J. (2000). Differential bacterial survival, replication, and apoptosis-inducing ability of Salmonella serovars within human and murine macrophages. Infect. Immun. 68, 1005-1013.
41. Shahnazari, S., Yen, W.-L., Birmingham, C. L., Shiu, J., Namolovan, A., Zheng, Y. T., Nakayama, K., Klionsky, D. J. and Brumell, J. H. (2010). A diacylglycerol-dependent signaling pathway contributes to regulation of antibacterial autophagy. Cell Host Microbe 8, 137-146.
42. Tam, M. A., Rydström, A., Sundquist, M. and Wick, M. J. (2008). Early cellular responses to Salmonella infection: dendritic cells, monocytes, and more. Immunol. Rev. 225, 140-162.
43. Tattoli, I., Philpott, D. J. and Girardin, S. E. (2012a). The bacterial and cellular determinants controlling the recruitment of mTOR to the Salmonella-containing vacuole. Biol. Open 1, 1215-1225.
44. Tattoli, I., Sorbara, M. T., Vuckovic, D., Ling, A., Soares, F., Carneiro, L. A., Yang, C., Emili, A., Philpott, D. J. and Girardin, S. E. (2012b). Amino acid starvation induced by invasive bacterial pathogens triggers an innate host defense program. Cell Host Microbe 11, 563-575.
45. Thurston, T. L., Ryzhakov, G., Bloor, S., von Muhlinen, N. and Randow, F. (2009). The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 10, 1215-1221.
46. Thurston, T. L. M., Wandel, M. P., von Muhlinen, N., Foeglein, A. and Randow, F. (2012). Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414-418.
47. Wild, P., Farhan, H., McEwan, D. G., Wagner, S., Rogov, V. V., Brady, N. R., Richter, B., Korac, J., Waidmann, O., Choudhary, C. et al. (2011). Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233.
48. Yu, H. B., Croxen, M. A., Marchiando, A. M., Ferreira, R. B., Cadwell, K., Foster, L. J. and Finlay, B. B. (2014). Autophagy facilitates Salmonella replication in HeLa cells. MBio 5, e00865-14.
49. Zhang, D. W., Jeang, K. T. and Lee, C. G. L. (2006). p53 negatively regulates the expression of FAT10, a gene upregulated in various cancers. Oncogene 25, 2318-2327.
50. Zheng, Y. T., Shahnazari, S., Brech, A., Lamark, T., Johansen, T. and Brumell, J. H. (2009). The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 183, 5909-5916.