Functional interaction of Heat Shock protein 90 and beclin 1 modulates toll-like receptor-mediated autophagy

FASEB Journal

Volumn 25, Issue 8, 2011, Pages 2700-2710

  Xu, Congfeng ^a   Liu, Jin ^a   Hsu, Li Chung ^b   Luo, Yunping ^c   Xiang, Rong ^d,e   Chuang, Tsung Hsien ^a,f  

^a BURNHAM INSTITUTE   (United States)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e NANKAI UNIVERSITY   (China)

^f NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

Innate immunity; Pattern recognition receptor; Ubiquitination

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BECLIN 1; BETA GALACTOSIDASE; COMPLEMENTARY DNA; CYCLOHEXIMIDE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; LACTACYSTIN; LUCIFERASE; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; PATTERN RECOGNITION RECEPTOR; PROTEASOME INHIBITOR; TOLL LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CONFOCAL MICROSCOPY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MONOCYTE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BENZOQUINONES; CELL LINE; EVOLUTION, MOLECULAR; HEK293 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, INNATE; INTERFERON-BETA; LACTAMS, MACROCYCLIC; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; NF-KAPPA B; PROTEIN INTERACTION DOMAINS AND MOTIFS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS; UBIQUITINATION;

EID: 80051688648     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-167676     Document Type: Article

References (56)

1. Imler, J. L., and Hoffmann, J. A. (2001) Toll receptors in innate immunity. Trends Cell Biol. 11, 304-311
2. Janeway, C. A., Jr., and Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216
3. Aderem, A., and Ulevitch, R. J. (2000) Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787
4. Chuang, T. H., and Ulevitch, R. J. (2001) Identification of hTLR10: a novel human Toll-like receptor preferentially expressed in immune cells. Biochim. Biophys. Acta 1518, 157-161
5. Kumar, H., Kawai, T., and Akira, S. (2009) Pathogen recognition in the innate immune response. Biochem. J. 420, 1-16
6. Beutler, B., Jiang, Z., Georgel, P., Crozat, K., Croker, B., Rutschmann, S., Du, X., and Hoebe, K. (2006) Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24, 353-389
7. West, A. P., Koblansky, A. A., and Ghosh, S. (2006) Recognition and signaling by toll-like receptors. Annu. Rev. Cell Dev. Biol. 22, 409-437
8. Lee, M. S., and Kim, Y. J. (2007) Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu. Rev. Biochem. 76, 447-480
9. O'Neill, L. A., and Bowie, A. G. (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7, 353-364 (Pubitemid 46674493)
10. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384
11. Xu, Y., Liu, X. D., Gong, X., and Eissa, N. T. (2008) Signaling pathway of autophagy associated with innate immunity. Autophagy 4, 110-112
12. Delgado, M. A., and Deretic, V. (2009) Toll-like receptors in control of immunological autophagy. Cell Death Differ. 16, 976-983
13. Mizushima, N., Levine, B., Cuervo, A. M., and Klionsky, D. J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (Pubitemid 351317450)
14. Levine, B., and Kroemer, G. (2008) Autophagy in the pathogenesis of disease. Cell 132, 27-42
15. Munz, C. (2009) Enhancing immunity through autophagy. Annu. Rev. Immunol. 27, 423-449
16. Huang, J., and Brumell, J. H. (2009) Autophagy in immunity against intracellular bacteria. Curr. Top. Microbiol. Immunol. 335, 189-215
17. Orvedahl, A., and Levine, B. (2009) Eating the enemy within: autophagy in infectious diseases. Cell Death Differ. 16, 57-69
18. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., and Green, D. R. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257
19. Xu, Y., Jagannath, C., Liu, X. D., Sharafkhaneh, A., Kolodziejska, K. E., and Eissa, N. T. (2007) Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 27, 135-144 (Pubitemid 47089027)
20. Delgado, M. A., Elmaoued, R. A., Davis, A. S., Kyei, G., and Deretic, V. (2008) Toll-like receptors control autophagy. EMBO J. 27, 1110-1121 (Pubitemid 351508141)
21. Shi, C. S., and Kehrl, J. H. (2008) MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 283, 33175-33182
22. Cao, Y., and Klionsky, D. J. (2007) Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res. 17, 839-849 (Pubitemid 47585112)
23. Sinha, S., and Levine, B. (2008) The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene 27(Suppl. 1), S137-S148
24. Deretic, V. (2009) Multiple regulatory and effector roles of autophagy in immunity. Curr. Opin. Immunol. 21, 53-62
25. He, C., and Klionsky, D. J. (2009) Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43, 67-93
26. Wandinger, S. K., Richter, K., and Buchner, J. (2008) The Hsp90 chaperone machinery. J. Biol. Chem. 283, 18473-18477
27. Pratt, W. B., Morishima, Y., and Osawa, Y. (2008) The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J. Biol. Chem. 283, 22885-22889
28. Pearl, L. H., Prodromou, C., and Workman, P. (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 410, 439-453 (Pubitemid 351429015)
29. Stravopodis, D. J., Margaritis, L. H., and Voutsinas, G. E. (2007) Drug-mediated targeted disruption of multiple protein activities through functional inhibition of the Hsp90 chaperone complex. Curr. Med. Chem. 14, 3122-3138 (Pubitemid 350226961)
30. Solit, D. B., and Chiosis, G. (2008) Development and application of Hsp90 inhibitors. Drug Discov. Today 13, 38-43
31. Kimura, S., Noda, T., and Yoshimori, T. (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460 (Pubitemid 47293726)
32. Lee, J., Hayashi, M., Lo, J. F., Fearns, C., Chu, W. M., Luo, Y., Xiang, R., and Chuang, T. H. (2009) Nuclear factor-κB (NF-κB) activation primes cells to a pro-inflammatory polarized response to a Toll-like receptor 7 (TLR7) agonist. Biochem. J. 421, 301-310
33. Kimura, S., Fujita, N., Noda, T., and Yoshimori, T. (2009) Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol. 452, 1-12
34. Birmingham, C. L., and Brumell, J. H. (2009) Methods to monitor autophagy of Salmonella enterica serovar Typhimurium. Methods Enzymol. 452, 325-343
35. Komander, D. (2009) The emerging complexity of protein ubiquitination. Biochem. Soc. Trans. 37, 937-953
36. Wertz, I. E., and Dixit, V. M. (2010) Regulation of death receptor signaling by the ubiquitin system. Cell Death Differ. 17, 14-24
37. Fearns, C., Pan, Q., Mathison, J. C., and Chuang, T. H. (2006) Triad3A regulates ubiquitination and proteasomal degradation of RIP1 following disruption of Hsp90 binding. J. Biol. Chem. 281, 34592-34600 (Pubitemid 46036665)
38. Kamynina, E., Kauppinen, K., Duan, F., Muakkassa, N., and Manor, D. (2007) Regulation of proto-oncogenic dbl by chaperone- controlled, ubiquitin-mediated degradation. Mol. Cell. Biol. 27, 1809-1822
39. Jeong, J. H., An, J. Y., Kwon, Y. T., Li, L. Y., and Lee, Y. J. (2008) Quercetin-induced ubiquitination and down-regulation of Her- 2/neu. J. Cell. Biochem. 105, 585-595
40. Ding, X., and Goldberg, M. S. (2009) Regulation of LRRK2 stability by the E3 ubiquitin ligase CHIP. PLoS One 4, e5949
41. Xiong, H., Li, H., Kong, H. J., Chen, Y., Zhao, J., Xiong, S., Huang, B., Gu, H., Mayer, L., Ozato, K., and Unkeless, J. C. (2005) Ubiquitin-dependent degradation of interferon regulatory factor-8 mediated by Cbl down-regulates interleukin-12 expression. J. Biol. Chem. 280, 23531-23539 (Pubitemid 40884831)
42. Chuang, T. H., Lee, J., Kline, L., Mathison, J. C., and Ulevitch, R. J. (2002) Toll-like receptor 9 mediates CpG-DNA signaling. J. Leukoc. Biol. 71, 538-544
43. Oshiumi, H., Matsumoto, M., Funami, K., Akazawa, T., and Seya, T. (2003) TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 4, 161-167 (Pubitemid 36193018)
44. Birmingham, C. L., and Brumell, J. H. (2006) Autophagy recognizes intracellular Salmonella enterica serovar Typhimurium in damaged vacuoles. Autophagy 2, 156-158 (Pubitemid 44030875)
45. Chang, Z. (2009) Posttranslational modulation on the biological activities of molecular chaperones. Sci. China C Life Sci. 52, 515-520
46. Blagosklonny, M. V. (2002) Hsp-90-associated oncoproteins: multiple targets of geldanamycin and its analogs. Leukemia 16, 455-462
47. Yang, K., Shi, H., Qi, R., Sun, S., Tang, Y., Zhang, B., and Wang, C. (2006) Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells. Mol. Biol. Cell 17, 1461-1471 (Pubitemid 43376563)
48. Fang, S., Fu, J., Yuan, X., Han, C., Shi, L., Xin, Y., Luo, L., and Yin, Z. (2009) Heat shock protein 90 regulates the stability of MEKK3 in HEK293 cells. Cell. Immunol. 259, 49-55
49. Shi, L., Zhang, Z., Fang, S., Xu, J., Liu, J., Shen, J., Fang, F., Luo, L., and Yin, Z. (2009) Heat shock protein 90 (Hsp90) regulates the stability of transforming growth factor beta-activated kinase 1 (TAK1) in interleukin-1β-induced cell signaling. Mol. Immunol. 46, 541-550
50. Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E. L., Mizushima, N., Ohsumi, Y., Cattoretti, G., and Levine, B. (2003) Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820 (Pubitemid 38063704)
51. Hsu, H. Y., Wu, H. L., Tan, S. K., Li, V. P., Wang, W. T., Hsu, J., and Cheng, C. H. (2007) Geldanamycin interferes with the 90-kDa heat shock protein, affecting lipopolysaccharide-mediated interleukin-1 expression and apoptosis within macrophages. Mol. Pharmacol. 71, 344-356 (Pubitemid 46021004)
52. Poulaki, V., Iliaki, E., Mitsiades, N., Mitsiades, C. S., Paulus, Y. N., Bula, D. V., Gragoudas, E. S., and Miller, J. W. (2007) Inhibition of Hsp90 attenuates inflammation in endotoxin-induced uveitis. FASEB J. 21, 2113-2123 (Pubitemid 47026447)
53. Shi, C. S., and Kehrl, J. H. (2010) TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci. Signal. 3, ra42
54. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R., Boone, D. L., Ma, A., Koonin, E. V., and Dixit, V. M. (2004) De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430, 694-699 (Pubitemid 39061687)
55. Korolchuk, V. I., Menzies, F. M., and Rubinsztein, D. C. (2010) Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 584, 1393-1398
56. Long, J., Gallagher, T. R., Cavey, J. R., Sheppard, P. W., Ralston, S. H., Layfield, R., and Searle, M. S. (2008) Ubiquitin recognition by the ubiquitin-associated domain of p62 involves a novel conformational switch. J. Biol. Chem. 283, 5427-5440