Loss of autophagy enhances MIF/macrophage migration inhibitory factor release by macrophages

Autophagy

Volumn 12, Issue 6, 2016, Pages 907-916

  Lee, Jacinta P W ^a   Foote, Andrew ^a   Fan, Huapeng ^a   Peral de Castro, Celia ^b   Lang, Tali ^a   Jones, Sarah A ^a   Gavrilescu, Nichita ^a   Mills, Kingston H G ^b   Leech, Michelle ^a   Morand, Eric F ^a   Harris, James ^a  

^a MONASH UNIVERSITY   (Australia)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

autophagosome; cytokines; inflammation; LPS; macrophage; reactive oxygen species; starvation

Indexed keywords

AUTOPHAGY PROTEIN 5; MACROPHAGE MIGRATION INHIBITION FACTOR; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; AMINO ACID;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE RELEASE; ESCHERICHIA COLI; HUMAN; HUMAN CELL; MACROPHAGE; MITOCHONDRIAL RESPIRATION; MONOCYTE; MOUSE; NONHUMAN; RAW 264.7 CELL LINE; REGULATORY MECHANISM; ANIMAL; DEFICIENCY; METABOLISM; MITOCHONDRION; SECRETION (PROCESS);

AMINO ACIDS; ANIMALS; AUTOPHAGY; HUMANS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MACROPHAGES; MICE; MITOCHONDRIA; RAW 264.7 CELLS; REACTIVE OXYGEN SPECIES;

EID: 84966697257     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1164358     Document Type: Article

References (43)

1. B.R.Bloom, B.Bennett. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 1966; 153:80-2; PMID:5938421; http://dx.doi.org/10.1126/science.153.3731.80
2. J.R.David. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 1966; 56:72-7; PMID:5229858; http://dx.doi.org/10.1073/pnas.56.1.72
3. M.Bozza, A.R.Satoskar, G.Lin, B.Lu, A.A.Humbles, C.Gerard, J.R.David. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 1999; 189:341-6; PMID:9892616; http://dx.doi.org/10.1084/jem.189.2.341
4. W.Y.Weiser, P.A.Temple, J.S.Witek-Giannotti, H.G.Remold, S.C.Clark, J.R.David. Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 1989; 86:7522-6; PMID:2552447; http://dx.doi.org/10.1073/pnas.86.19.7522
5. J.Bernhagen, T.Calandra, R.A.Mitchell, S.B.Martin, K.J.Tracey, W.Voelter, K.R.Manogue, A.Cerami, R.Bucala. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993; 365:756-9; PMID:8413654; http://dx.doi.org/10.1038/365756a0
6. H.Y.Lan. Role of macrophage migration inhibition factor in kidney disease. Nephron Exp Nephrol 2008; 109:e79–83; PMID:18663334; http://dx.doi.org/10.1159/000145463
7. T.Calandra, J.Bernhagen, R.A.Mitchell, R.Bucala. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 1994; 179:1895-902; PMID:8195715; http://dx.doi.org/10.1084/jem.179.6.1895
8. J.Bernhagen, R.A.Mitchell, T.Calandra, W.Voelter, A.Cerami, R.Bucala. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry 1994; 33:14144-55; PMID:7947826; http://dx.doi.org/10.1021/bi00251a025
9. F.Q.Cunha, D.W.Moss, L.M.Leal, S.Moncada, F.Y.Liew. Induction of macrophage parasiticidal activity by Staphylococcus aureus and exotoxins through the nitric oxide synthesis pathway. Immunology 1993; 78:563-7; PMID:8495974
10. S.Onodera, K.Suzuki, T.Matsuno, K.Kaneda, M.Takagi, J.Nishihira. Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 1997; 92:131-7; PMID:9370935; http://dx.doi.org/10.1046/j.1365-2567.1997.00311.x
11. T.Roger, J.Delaloye, A.L.Chanson, M.Giddey, D.Le Roy, T.Calandra. Macrophage migration inhibitory factor deficiency is associated with impaired killing of gram-negative bacteria by macrophages and increased susceptibility to Klebsiella pneumoniae sepsis. J Infect Dis 2013; 207:331-9; PMID:23125447; http://dx.doi.org/10.1093/infdis/jis673
12. A.Foote, E.M.Briganti, Y.Kipen, L.Santos, M.Leech, E.F.Morand. Macrophage migration inhibitory factor in systemic lupus erythematosus. J Rheumatol 2004; 31:268-73; PMID:14760795
13. E.F.Morand, M.Leech, J.Bernhagen. MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov 2006; 5:399-410; PMID:16628200; http://dx.doi.org/10.1038/nrd2029
14. K.Buffen, M.Oosting, S.Mennens, P.K.Anand, T.S.Plantinga, P.Sturm, F.L.van de Veerdonk, J.W.van der Meer, R.J.Xavier, T.D.Kanneganti, et al. Autophagy modulates Borrelia burgdorferi-induced production of interleukin-1beta (IL-1beta). J Biol Chem 2013; 288:8658-66; PMID:23386602; http://dx.doi.org/10.1074/jbc.M112.412841
15. J.Harris, M.Hartman, C.Roche, S.G.Zeng, A.O'Shea, F.A.Sharp, E.M.Lambe, E.M.Creagh, D.T.Golenbock, J.Tschopp, et al. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem 2011; 286:9587-97; PMID:21228274; http://dx.doi.org/10.1074/jbc.M110.202911
16. J.Henault, J.Martinez, J.M.Riggs, J.Tian, P.Mehta, L.Clarke, M.Sasai, E.Latz, M.M.Brinkmann, A.Iwasaki, et al. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 2012; 37:986-97; PMID:23219390; http://dx.doi.org/10.1016/j.immuni.2012.09.014
17. T.Saitoh, N.Fujita, M.H.Jang, S.Uematsu, B.G.Yang, T.Satoh, H.Omori, T.Noda, N.Yamamoto, M.Komatsu, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456:264-8; PMID:18849965; http://dx.doi.org/10.1038/nature07383
18. M.C.Tal, M.Sasai, H.K.Lee, B.Yordy, G.S.Shadel, A.Iwasaki. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci USA 2009; 106:2770-5; PMID:19196953; http://dx.doi.org/10.1073/pnas.0807694106
19. C.Peral de Castro, S.A.Jones, C.Ni Cheallaigh, C.A.Hearnden, L.Williams, J.Winter, E.C.Lavelle, K.H.Mills, J.Harris. Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion. J Immunol 2012; 189:4144-53; http://dx.doi.org/10.4049/jimmunol.1201946
20. E.F.Castillo, A.Dekonenko, J.Arko-Mensah, M.A.Mandell, N.Dupont, S.Jiang, M.Delgado-Vargas, G.S.Timmins, D.Bhattacharya, H.Yang, et al. Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad Sci USA 2012; 109:E3168-76; PMID:23093667; http://dx.doi.org/10.1073/pnas.1210500109
21. X.Xu, Y.Hua, S.Nair, R.Bucala, J.Ren. Macrophage migration inhibitory factor deletion exacerbates pressure overload-induced cardiac hypertrophy through mitigating autophagy. Hypertension 2014; 63:490-9; PMID:24366076; http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.02219
22. X.Xu, B.D.Pacheco, L.Leng, R.Bucala, J.Ren. Macrophage migration inhibitory factor plays a permissive role in the maintenance of cardiac contractile function under starvation through regulation of autophagy. Cardiovasc Res 2013; 99:412-21; PMID:23674514; http://dx.doi.org/10.1093/cvr/cvt116
23. H.R.Chen, Y.C.Chuang, C.H.Chao, T.M.Yeh. Macrophage migration inhibitory factor induces vascular leakage via autophagy. Biol Open 2015; 4:244-52; PMID:25617421; http://dx.doi.org/10.1242/bio.201410322
24. Y.C.Chuang, W.H.Su, H.Y.Lei, Y.S.Lin, H.S.Liu, C.P.Chang, T.M.Yeh. Macrophage migration inhibitory factor induces autophagy via reactive oxygen species generation. PloS One 2012; 7:e37613; PMID:22629429; http://dx.doi.org/10.1371/journal.pone.0037613
25. Y.Liu, L.Zhao, Y.Ju, W.Li, M.Zhang, Y.Jiao, J.Zhang, S.Wang, Y.Wang, M.Zhao, et al. A novel androstenedione derivative induces ROS-mediated autophagy and attenuates drug resistance in osteosarcoma by inhibiting macrophage migration inhibitory factor (MIF). Cell Death Dis 2014; 5:e1361; PMID:25101674; http://dx.doi.org/10.1038/cddis.2014.300
26. M.Y.Wu, J.Fu, J.Xu, B.W.O'Malley, R.C.Wu. Steroid receptor coactivator 3 regulates autophagy in breast cancer cells through macrophage migration inhibitory factor. Cell Res 2012; 22:1003-21; PMID:22430150; http://dx.doi.org/10.1038/cr.2012.44
27. X.Xu, J.Ren. Macrophage migration inhibitory factor (MIF) knockout preserves cardiac homeostasis through alleviating Akt-mediated myocardial autophagy suppression in high-fat diet-induced obesity. Int J Obes 2015; 39:387-96; PMID:25248618; http://dx.doi.org/10.1038/ijo.2014.174
28. K.Nakahira, J.A.Haspel, V.A.Rathinam, S.J.Lee, T.Dolinay, H.C.Lam, J.A.Englert, M.Rabinovitch, M.Cernadas, H.P.Kim, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12:222-30; PMID:21151103; http://dx.doi.org/10.1038/ni.1980
29. R.Zhou, A.S.Yazdi, P.Menu, J.Tschopp. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469:221-5; PMID:21124315; http://dx.doi.org/10.1038/nature09663
30. N.Dupont, S.Jiang, M.Pilli, W.Ornatowski, D.Bhattacharya, V.Deretic. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1beta. EMBO J 2011; 30:4701-11; PMID:22068051; http://dx.doi.org/10.1038/emboj.2011.398
31. M.Zhang, S.Kenny, L.Ge, K.Xu, R.Schekman. Translocation of interleukin-1beta into a vesicle intermediate in autophagy-mediated secretion. Elife 2015; 4:e11205.
32. P.Pelegrin, C.Barroso-Gutierrez, A.Surprenant. P2´7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J Immunol 2008; 180:7147-57; http://dx.doi.org/10.4049/jimmunol.180.11.7147
33. M.Merk, J.Baugh, S.Zierow, L.Leng, U.Pal, S.J.Lee, A.D.Ebert, Y.Mizue, J.O.Trent, R.Mitchell, et al. The Golgi-associated protein p115 mediates the secretion of macrophage migration inhibitory factor. J Immunol 2009; 182:6896-906; http://dx.doi.org/10.4049/jimmunol.0803710
34. M.Sohda, Y.Misumi, A.Yano, N.Takami, Y.Ikehara. Phosphorylation of the vesicle docking protein p115 regulates its association with the Golgi membrane. J Biol Chem 1998; 273:5385-8; PMID:9478999; http://dx.doi.org/10.1074/jbc.273.9.5385
35. O.Flieger, A.Engling, R.Bucala, H.Lue, W.Nickel, J.Bernhagen. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett 2003; 551:78-86; PMID:12965208; http://dx.doi.org/10.1016/S0014-5793(03)00900-1
36. K.Nagao, M.Maeda, N.B.Manucat, K.Ueda. Cyclosporine A and PSC833 inhibit ABCA1 function via direct binding. Biochim Biophys Acta 2013; 1831:398-406; PMID:23153588; http://dx.doi.org/10.1016/j.bbalip.2012.11.002
37. U.Arndt, G.Wennemuth, P.Barth, M.Nain, Y.Al-Abed, A.Meinhardt, D.Gemsa, M.Bacher. Release of macrophage migration inhibitory factor and CXCL8/interleukin-8 from lung epithelial cells rendered necrotic by influenza A virus infection. J Virol 2002; 76:9298-306; PMID:12186913; http://dx.doi.org/10.1128/JVI.76.18.9298-9306.2002
38. C.S.Shi, J.H.Kehrl. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J Biol Chem 2008; 283:33175-82; PMID:18772134; http://dx.doi.org/10.1074/jbc.M804478200
39. T.Lang, A.Foote, J.Lee, E.F.Morand, J.Harris. MIF: Implications in the patho-aetiology of systemic lupus erythematosus. Front Immunol 2015; 6:577.
40. J.Candido, T.Hagemann. Cancer-related inflammation. J Clin Immunol 2013; 33(Suppl 1):S79-84; PMID:23225204; http://dx.doi.org/10.1007/s10875-012-9847-0
41. S.A.Jones, K.H.Mills, J.Harris. Autophagy and inflammatory diseases. Immunol Cell Biol 2013; 91:250-8; PMID:23318657; http://dx.doi.org/10.1038/icb.2012.82
42. J.Harris, S.A.De Haro, S.S.Master, J.Keane, E.A.Roberts, M.Delgado, V.Deretic. T helper 2 cytokines inhibit autophagic control of intracellular Mycobacterium tuberculosis. Immunity 2007; 27:505-17; PMID:17892853; http://dx.doi.org/10.1016/j.immuni.2007.07.022
43. R.Gu, L.L.Santos, D.Ngo, H.Fan, P.P.Singh, G.Fingerle-Rowson, R.Bucala, J.Xu, J.M.Quinn, E.F.Morand. Macrophage migration inhibitory factor is essential for osteoclastogenic mechanisms in vitro and in vivo mouse model of arthritis. Cytokine 2015; 72:135-45; PMID:25647268; http://dx.doi.org/10.1016/j.cyto.2014.11.015