Mycotoxin patulin suppresses innate immune responses by mitochondrial dysfunction and p62/sequestosome-1-dependent mitophagy

Journal of Biological Chemistry

Volumn 291, Issue 37, 2016, Pages 19299-19311

  Tsai, Wan Ting ^a   Lo, Yin Chiu ^a   Wu, Ming Sian ^a   Li, Chia Yang ^a,b   Kuo, Yi Ping ^a   Lai, Yi Hui ^c   Tsai, Yu ^a   Chen, Kai Chieh ^a   Chuang, Tsung Hsien ^a   Ya, Chun Hsu ^a   Lee, Jinq Chyi ^a   Hsu, Li Chung ^c   Hsu, John T A ^a   Yu, Guann Yi ^a,d  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; PATHOLOGY; PATTERN RECOGNITION;

ADAPTIVE IMMUNE RESPONSE; CYTOKINE PRODUCTION; DISEASE PROGRESSION; HEPATOCELLULAR CARCINOMA; INNATE IMMUNE RESPONSE; MITOCHONDRIAL DYSFUNCTION; PATTERN RECOGNITION RECEPTORS; TOLL-LIKE RECEPTORS;

IMMUNE SYSTEM;

CYTOKINE; GLUTATHIONE; PATULIN; PROTEIN P62; RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I LIKE RECEPTOR; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; MYCOTOXIN; SEQUESTOSOME 1; SQSTM1 PROTEIN, HUMAN; SQSTM1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INFLAMMATION; INNATE IMMUNITY; MITOPHAGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; DRUG EFFECTS; HEK293 CELL LINE; IMMUNOLOGY; RAW 264.7 CELL LINE;

ANIMALS; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; MICE; MITOCHONDRIAL DEGRADATION; MYCOTOXINS; PATULIN; RAW 264.7 CELLS; SEQUESTOSOME-1 PROTEIN;

EID: 84986877476     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.686683     Document Type: Article

References (55)

1. Iwasaki, A., and Medzhitov, R. (2015) Control of adaptive immunity by the innate immune system. Nat. Immunol. 16, 343-353
2. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820
3. Fukata, M., and Abreu, M. T. (2008) Role of Toll-like receptors in gastrointestinal malignancies. Oncogene 27, 234-243
4. Castello, G., Scala, S., Palmieri, G., Curley, S. A., and Izzo, F. (2010) HCV-related hepatocellular carcinoma: from chronic inflammation to cancer. Clin. Immunol. 134, 237-250
5. Horner, S. M., and Gale, M., Jr. (2013) Regulation of hepatic innate immunity by hepatitis C virus. Nat. Med. 19, 879-888
6. Wang, J. Q., Jeelall, Y. S., Ferguson, L. L., and Horikawa, K. (2014) Toll-like receptors and cancer: MYD88 mutation and inflammation. Front. Immunol. 5, 367
7. Castello, G., Costantini, S., and Scala, S. (2010) Targeting the inflammation in HCV-associated hepatocellular carcinoma: a role in the prevention and treatment. J. Transl. Med. 8, 109
8. Lee, J. Y., Zhao, L., and Hwang, D. H. (2010) Modulation of pattern recognition receptor-mediated inflammation and risk of chronic diseases by dietary fatty acids. Nutr. Rev. 68, 38-61
9. He, G., Yu, G. Y., Temkin, V., Ogata, H., Kuntzen, C., Sakurai, T., Sieghart, W., Peck-Radosavljevic, M., Leffert, H. L., and Karin, M. (2010) Hepatocyte IKKβ/NF-κB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 17, 286-297
10. Naugler, W. E., Sakurai, T., Kim, S., Maeda, S., Kim, K., Elsharkawy, A. M., and Karin, M. (2007) Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317, 121-124
11. Rebouissou, S., Amessou, M., Couchy, G., Poussin, K., Imbeaud, S., Pilati, C., Izard, T., Balabaud, C., Bioulac-Sage, P., and Zucman-Rossi, J. (2009) Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours. Nature 457, 200-204
12. Capone, F., Costantini, S., Guerriero, E., Calemma, R., Napolitano, M., Scala, S., Izzo, F., and Castello, G. (2010) Serum cytokine levels in patients with hepatocellular carcinoma. Eur. Cytokine Netw. 21, 99-104
13. Yu, G. Y., He, G., Li, C. Y., Tang, M., Grivennikov, S., Tsai, W. T., Wu, M. S., Hsu, C. W., Tsai, Y., Wang, L. H., and Karin, M. (2012) Hepatic expression of HCV RNA-dependent RNA polymerase triggers innate immune signaling and cytokine production. Mol. Cell 48, 313-321
14. Boyd, E. M. (1944) Patulin. Can. Med. Assoc. J. 50, 159
15. Fliege, R., and Metzler, M. (2000) Electrophilic properties of patulin: N-acetylcysteine and glutathione adducts. Chem. Res. Toxicol. 13, 373-381
16. Burghardt, R. C., Barhoumi, R., Lewis, E. H., Bailey, R. H., Pyle, K. A., Clement, B. A., and Phillips, T. D. (1992) Patulin-induced cellular toxicity: a vital fluorescence study. Toxicol. Appl. Pharmacol. 112, 235-244
17. Barhoumi, R., and Burghardt, R. C. (1996) Kinetic analysis of the chronology of patulin- and gossypol-induced cytotoxicity in vitro. Fundam. Appl. Toxicol. 30, 290-297
18. Zhang, B., Peng, X., Li, G., Xu, Y., Xia, X., and Wang, Q. (2015) Oxidative stress is involved in Patulin induced apoptosis in HEK293 cells. Toxicon 94, 1-7
19. Wu, T. S., Liao, Y. C., Yu, F. Y., Chang, C. H., and Liu, B. H. (2008) Mechanism of patulin-induced apoptosis in human leukemia cells (HL-60). Toxicol. Lett. 183, 105-111
20. Kwon, O., Soung, N. K., Thimmegowda, N. R., Jeong, S. J., Jang, J. H., Moon, D. O., Chung, J. K., Lee, K. S., Kwon, Y. T., Erikson, R. L., Ahn, J. S., and Kim, B. Y. (2012) Patulin induces colorectal cancer cells apoptosis through EGR-1 dependent ATF3 up-regulation. Cell. Signal. 24, 943-950
21. Fribley, A. M., Cruz, P. G., Miller, J. R., Callaghan, M. U., Cai, P., Narula, N., Neubig, R. R., Showalter, H. D., Larsen, S. D., Kirchhoff, P. D., Larsen, M. J., Burr, D. A., Schultz, P. J., Jacobs, R. R., Tamayo-Castillo, G., et al. (2011) Complementary cell-based high-throughput screens identify novel modulators of the unfolded protein response. J. Biomol. Screen. 16, 825-835
22. Boussabbeh, M., Ben Salem, I., Prola, A., Guilbert, A., Bacha, H., Abid-Essefi, S., and Lemaire, C. (2015) Patulin induces apoptosis through ROSmediated endoplasmic reticulum stress pathway. Toxicol. Sci. 144, 328-337
23. Doi, K., and Uetsuka, K. (2014) Mechanisms of mycotoxin-induced dermal toxicity and tumorigenesis through oxidative stress-related pathways. J. Toxicol. Pathol. 27, 1-10
24. Marin, M. L., Murtha, J., Dong, W., and Pestka, J. J. (1996) Effects of mycotoxins on cytokine production and proliferation in EL-4 thymoma cells. J. Toxicol. Environ. Health 48, 379-396
25. Luft, P., Oostingh, G. J., Gruijthuijsen, Y., Horejs-Hoeck, J., Lehmann, I., and Duschl, A. (2008) Patulin influences the expression of Th1/Th2 cytokines by activated peripheral blood mononuclear cells and T cells through depletion of intracellular glutathione. Environ. Toxicol. 23, 84-95
26. Yu, H. B., and Finlay, B. B. (2008) The caspase-1 inflammasome: a pilot of innate immune responses. Cell Host Microbe 4, 198-208
27. Pelegrin, P., Barroso-Gutierrez, C., and Surprenant, A. (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J. Immunol. 180, 7147-7157
28. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., and Lee, J. O. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130, 1071-1082
29. Kang, J. Y., Nan, X., Jin, M. S., Youn, S. J., Ryu, Y. H., Mah, S., Han, S. H., Lee, H., Paik, S. G., and Lee, J. O. (2009) Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31, 873-884
30. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745
31. 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
32. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
33. Perry, S. W., Norman, J. P., Barbieri, J., Brown, E. B., and Gelbard, H. A. (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques 50, 98-115
34. Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., and Springer, W. (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131
35. Okatsu, K., Saisho, K., Shimanuki, M., Nakada, K., Shitara, H., Sou, Y. S., Kimura, M., Sato, S., Hattori, N., Komatsu, M., Tanaka, K., and Matsuda, N. (2010) p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria. Genes Cells 15, 887-900
36. Randow, F., and Youle, R. J. (2014) Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe 15, 403-411
37. Seglen, P. O., and Gordon, P. B. (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U.S.A. 79, 1889-1892
38. Allen, G. F., Toth, R., James, J., and Ganley, I. G. (2013) Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 14, 1127-1135
39. Jain, A., Lamark, T., Sjøttem, E., Larsen, K. B., Awuh, J. A., øvervatn, A., McMahon, M., Hayes, J. D., and Johansen, T. (2010) p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 285, 22576-22591
40. Kim, J. Y., and Ozato, K. (2009) The sequestosome 1/p62 attenuates cytokine gene expression in activated macrophages by inhibiting IFN regulatory factor 8 and TNF receptor-associated factor 6/NF-κB activity. J. Immunol. 182, 2131-2140
41. Fujita, K., Maeda, D., Xiao, Q., and Srinivasula, S. M. (2011) Nrf2-mediated induction of p62 controls Toll-like receptor-4-driven aggresome-like induced structure formation and autophagic degradation. Proc. Natl. Acad. Sci. U.S.A. 108, 1427-1432
42. Moscat, J., Diaz-Meco, M. T., and Wooten, M. W. (2007) Signal integration and diversification through the p62 scaffold protein. Trends Biochem. Sci. 32, 95-100
43. Häcker, H., Vabulas, R. M., Takeuchi, O., Hoshino, K., Akira, S., and Wagner, H. (2000) Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptorassociated factor (TRAF)6. J. Exp. Med. 192, 595- 600
44. Sanz, L., Diaz-Meco, M. T., Nakano, H., and Moscat, J. (2000) The atypical PKC-interacting protein p62 channels NF-κB activation by the IL-1-TRAF6 pathway. EMBO J. 19, 1576-1586
45. East, D. A., Fagiani, F., Crosby, J., Georgakopoulos, N. D., Bertrand, H., Schaap, M., Fowkes, A., Wells, G., and Campanella, M. (2014) PMI: a DeltaPsim independent pharmacological regulator of mitophagy. Chem. Biol. 21, 1585-1596
46. Hatey, F., and Moulé, Y. (1979) Protein synthesis inhibition in rat liver by the mycotoxin patulin. Toxicology 13, 223-231
47. Arafat, W., and Musa, M. N. (1995) Patulin-induced inhibition of protein synthesis in hepatoma tissue culture. Res. Commun. Mol. Pathol. Pharmacol. 87, 177-186
48. Breitbart, H. (1981) Effect of ionophores and metabolic inhibitors on protein synthesis in rabbit reticulocytes. Biochim. Biophys. Acta 656, 160-166
49. Otero, M. J., and Carrasco, L. (1984) Action of oligomycin on cultured mammalian cells: permeabilization to translation inhibitors. Mol. Cell. Biochem. 61, 183-191
50. West, A. P., Shadel, G. S., and Ghosh, S. (2011) Mitochondria in innate immune responses. Nat. Rev. Immunol. 11, 389-402
51. Iyer, S. S., He, Q., Janczy, J. R., Elliott, E. I., Zhong, Z., Olivier, A. K., Sadler, J. J., Knepper-Adrian, V., Han, R., Qiao, L., Eisenbarth, S. C., Nauseef, W. M., Cassel, S. L., and Sutterwala, F. S. (2013) Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 39, 311-323
52. West, A. P., Brodsky, I. E., Rahner, C., Woo, D. K., Erdjument-Bromage, H., Tempst, P., Walsh, M. C., Choi, Y., Shadel, G. S., and Ghosh, S. (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472, 476-480
53. Seth, R. B., Sun, L., Ea, C. K., and Chen, Z. J. (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122, 669-682
54. Liu, S., Chen, J., Cai, X., Wu, J., Chen, X., Wu, Y. T., Sun, L., and Chen, Z. J. (2013) MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades. eLife 2, e00785
55. Zhang, X., Goncalves, R., and Mosser, D. M. (2008) The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. 10.1002/0471142735.im1401s83