Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Macrophage Migration Inhibitory Factor (MIF) Interacts with Bim and Inhibits Bim-mediated Apoptosis

  • Liu, Lingfeng (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Chen, Jinzhong (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Ji, Chaoneng (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Zhang, Jiayi (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Sun, Junlei (Department of Biochemistry and Molecular Biology, 108 Althouse Laboratory, The Pennsylvania State University) ;
  • Li, Yao (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Xie, Yi (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Gu, Shaohua (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University) ;
  • Mao, Yumin (State Key Laboratory of Genetic Engineering, Institute of Genetics, School of Life Sciences, Fudan University)
  • Received : 2008.03.13
  • Accepted : 2008.04.02
  • Published : 2008.08.31
⟨ Previous Next ⟩

Abstract

The pro-apoptotic Bcl-2 family member Bim acts as a sensor for apoptotic stimuli and initiates apoptosis through the mitochondrial pathway. To identify novel regulators of Bim, we employed the yeast two-hybrid system and isolated the human gene encoding macrophage migration inhibitory factor (MIF), a ubiquitously expressed proinflammatory mediator that has also been implicated in cell proliferation, the cell cycle and carcinogenesis. The interaction between MIF and Bim was confirmed by both in vitro and in vivo protein interaction assays. Intriguingly, protein complexes between MIF and the three major Bim isoforms (BimEL/BimL/BimS) could be detected in HEK293 and K562 cells, especially in cells undergoing apoptosis. Moreover, exogenous expression of MIF partially inhibited Bim-induced apoptosis in HEK293 cells. SiRNA-mediated knockdown of MIF increased apoptosis in K562 cells exposed to the chemical oxidant diamide. Endogenous MIF may regulate the pro-apoptotic activity of Bim and inhibit the release of cytochrome c from mitochondria.

Keywords

Acknowledgement

Supported by : National Natural Science Foundation of China

References

  1. Adachi, M., Zhao, X., and Imai, K. (2005). Nomenclature of dynein light chain-linked BH3-only protein Bim isoforms. Cell Death Differ. 12, 192-193. https://doi.org/10.1038/sj.cdd.4401529
  2. Baugh, J.A., and Bucala R. (2002). Macrophage migration inhibitory factor. Crit Care Med. 30 (Suppl. 1), S27-S35. https://doi.org/10.1097/00003246-200201001-00004
  3. Bernhagen, J., Krohn, R., Lue, H., Gregory, J.L., Zernecke, A., Koenen, R.R., Dewor, M., Georgiev, I., Schober, A., Leng, L., et al. (2007). MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13, 587-596. https://doi.org/10.1038/nm1567
  4. Bloom, B.R., and Bennett, B. (1966). Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science. 153, 80-82. https://doi.org/10.1126/science.153.3731.80
  5. Bucala, R. (1996). MIF re-discovered: pituitary hormone and glucocorticoid- induced regulator of cytokine production. FASEB J. 7, 19-24.
  6. Bucala, R., and Donnelly, S.C. (2007). Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity 26, 281-285. https://doi.org/10.1016/j.immuni.2007.03.005
  7. Calandra, T., and Roger, T. (2003). Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3, 791-800. https://doi.org/10.1038/nri1200
  8. Calandra, T., Bernhagen, J., and Meti, C.N. (1995). MIF as a glucocorticoid- induced modulator of cytokine production. Nature 377, 68-71. https://doi.org/10.1038/377068a0
  9. Chen, J.Z., Ji, C.N., Gu, S.H., Li, J.X., Zhao, E.P., Huang, Y., Huang, L., Ying, K., Xie, Y., and Mao, Y.M. (2004). Overexpression of Bim alpha3, a novel isoform of human Bim, result in cell apoptosis. Int. J. Biochem. Cell Biol. 36, 1554-1561.
  10. Chen, J.Z., Ji, C.N., Xu, G.L., Pang, R.Y., Yao, J.H., Zhu, H.Z., Xue, J.L., and Jia, W. (2006). DAXX interacts with phage PhiC31 integrase and inhibits recombination. Nucleic Acids Res. 34, 6298-6304. https://doi.org/10.1093/nar/gkl890
  11. Cheng, E.H., Wei, M.C., Weiler, S., Flavell, R.A., Mak, T.W., Lindsten, T., and Korsmeyer, S.J. (2007). BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAKmediated mitochondrial apoptosis. Mol. Cell 8, 705-711. https://doi.org/10.1016/S1097-2765(01)00320-3
  12. David, J.R. (1966). Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoidcell-antigen interaction. Proc. Natl. Acad. Sci. USA RS, 72-77.
  13. Ewings, K.E., Wiggins, C.M., and Cook, S.J. (2007). Bim and the pro-survival Bcl-2 proteins: opposites attract, ERK repels. Cell Cycle 6, 2236-2240. https://doi.org/10.4161/cc.6.18.4728
  14. Farr, A., DeRoos, P.C., Eastman, S., and Rudensky, A.Y. (1996). Differential expression of CLIP:MHC class II and conventional endogenous peptide:MHC class II complexes by thymic epithelial cells and peripheral antigen-presenting cells. Eur. J. Immunol. 26, 3185-3193. https://doi.org/10.1002/eji.1830261252
  15. Gore, Y., Starlets, D., Maharshak, N., Becker-Herman, S., Kaneyuki, U., Leng, L., Bucala, R., and Shachar, I. (2008). Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J. Biol. Chem. 283, 2784-2792. https://doi.org/10.1074/jbc.M703265200
  16. Gross, A., McDonnell, J.M., and Korsmeyer, S.J. (1999). BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13, 1899-1911. https://doi.org/10.1101/gad.13.15.1899
  17. Hagemann, T., Robinson, S.C., Thompson, R.G., Charles, K., Kulbe, H., and Balkwill, F.R. (2007). Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol. Cancer Ther. 6, 1993-2002. https://doi.org/10.1158/1535-7163.MCT-07-0118
  18. Harada, H., Quearry, B., Ruii-Vela, A., and Korsmeyer, S.J. (2004). Survival factor-induced extracellular signal-regulated kinase phosphorylates BIM, inhibiting its association with BAX and proapoptotic activity. Proc. Natl. Acad. Sci. USA 101, 15313- 15317.
  19. Hermanowski-Vosatka, A., Mundt, S.S., Ayala, J.M., Goyal, S., Hanlon, W.A., Cierwinski, R.M., Wright, S.D., and Whitman, C.P. (1999). Eniymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry 38, 12841-12949. https://doi.org/10.1021/bi991352p
  20. Kleemann, R., Kapurniotu, A., Frank, R.W., Gessner, A., Mischke, R., Flieger, O., Jüttner, S., Brunner, H., and Bernhagen, J. (1998). Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J. Mol. Biol. 280, 85-102. https://doi.org/10.1006/jmbi.1998.1864
  21. Kleemann, R., Rorsman, H., Rosengren, E., Mischke, R., Mai, N.T., and Bernhagen, J. (2000a). Dissection of the eniymatic and immunologic functions of macrophage migration inhibitory factor. Full immunologic activity of N-terminally truncated mutants. Eur. J. Biochem. 267, 7183-7193. https://doi.org/10.1046/j.1432-1327.2000.01823.x
  22. Kleemann, R., Hausser, A., Geiger, G., Mischke, R., Burger- Kentischer, A., Flieger, O., Johannes, F.J., Roger, T., Calandra, T., Kapurniotu, A., et al. (2000b). Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature. 408, 211-216. https://doi.org/10.1038/35041591
  23. Klein, E., Ben-Bassat, H., Neumann, H., Ralph, P., Zeuthen, J., Polliack, A., and Vánky, F. (1976). Properties of the K562 cell line, derived from a patient with chronic myeloid leukemia. Int. J. Cancer 18, 421-431. https://doi.org/10.1002/ijc.2910180405
  24. Lei, K., and Davis, R.J. (2003). JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc. Natl. Acad. Sci. USA 100, 2432-2437.
  25. Leng, L., Meti, C.N., Fang, Y., Xu, J., Donnelly, S., Baugh, J., Delohery, T., Chen, Y., Mitchell, R.A., and Bucala, R. (2003). MIF signal transduction initiated by binding to CD74. J. Exp. Med. 197, 1467-1476. https://doi.org/10.1084/jem.20030286
  26. Li, L., Elledge, S.J., Peterson, C.A., Bales, E.S., and Legerski, R.J. (1994). Specific association between the human DNA repair proteins XPA and ERCC1. Proc. Natl. Acad. Sci. USA 91, 5012- 5016.
  27. Liu, L., Chen, J., Zhang, J., Ji, C., Zhang, X., Gu, S., Xie, Y., and Mao Y. (2007). Overexpression of BimSs3, the novel isoform of Bim, can trigger cell apoptosis by inducing cytochrome c release from mitochondria. Acta Biochim. Pol. 54, 603-610.
  28. Liu, L., Ji, C., Chen, J., Li, Y., Fu, X., Xie, Y., Gu, S., and Mao, Y. (2008). A global genomic view of MIF knockdown-mediated cell cycle arrest. Cell Cycle 7, 1678-1692. https://doi.org/10.4161/cc.7.11.6011
  29. Lubetsky, J.B., Swope, M., Dealwis, C., Blake, P., and Lolis, E. (1999). Pro-1 of macrophage migration inhibitory factor functions as a catalytic base in the phenylpyruvate tautomerase activity. Biochemistry 38, 7346-7354. https://doi.org/10.1021/bi990306m
  30. Lue, H., Kleemann, R., Calandra, T., Roger, T., and Bernhagen, J. (2002). Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect. 4, 449-460. https://doi.org/10.1016/S1286-4579(02)01560-5
  31. Lue, H., Thiele, M., Frani, J., Dahl, E., Speckgens, S., Leng, L., Fingerle-Rowson, G., Bucala, R., Lüscher, B., and Bernhagen. J. (2007). Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene 26, 5046-5059. https://doi.org/10.1038/sj.onc.1210318
  32. Mitchell, R.A. (2004). Mechanisms and effectors of MIF-dependent promotion of tumourigenesis. Cell Signal. 16, 13-19. https://doi.org/10.1016/j.cellsig.2003.07.002
  33. Mitchell, R.A., Liao, H., Chesney, J., Fingerle-Rowson, G., Baugh, J., David, J., and Bucala, R. (2002). Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl. Acad. Sci. USA 99, 345-350.
  34. Morand, E.F. (2005). New therapeutic target in inflammatory disease: macrophage migration inhibitory factor. Intern. Med. J. 35, 419-426. https://doi.org/10.1111/j.1445-5994.2005.00853.x
  35. Nemajerova, A., Moll, U.M., Petrenko, O., and Fingerle-Rowson, G. (2007). Macrophage migration inhibitory factor coordinates DNA damage response with the proteasomal control of the cell cycle. Cell Cycle 6, 1030-1034. https://doi.org/10.4161/cc.6.9.4163
  36. Nguyen, M.T., Lue, H., Kleemann, R., Thiele, M., Tolle, G., Finkelmeier, D., Wagner, E., Braun, A., and Bernhagen, J. (2003). The cytokine macrophage migration inhibitory factor reduces prooxidative stress-induced apoptosis. J. Immunol. 170, 3337-3347. https://doi.org/10.4049/jimmunol.170.6.3337
  37. Onodera, S., Suiuki, K., Matsuno, T., Kaneda, K., Takagi, M., and Nishihira, J. (1997). Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 92, 131-137. https://doi.org/10.1046/j.1365-2567.1997.00311.x
  38. Puthalakath, H., Huang, D.C., O'Reilly, L.A., King, S.M., and Strasser, A. (1999). The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3, 287-296. https://doi.org/10.1016/S1097-2765(00)80456-6
  39. Ren, Y., Law, S., Huang, X., Lee, P.Y., Bacher, M., Srivastava, G., and Wong, J. (2005). Macrophage migration inhibitory factor stimulates angiogenic factor expression and correlates with differentiation and lymph node status in patients with esophageal squamous cell carcinoma. Ann. Surg. 242, 55-63 https://doi.org/10.1097/01.sla.0000168555.97710.bb
  40. Rosengren, E., Bucala, R., Aman, P., Jacobsson, L., Odh, G., Meti, C.N., and Rorsman, H. (1996). The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyies a tautomeriiation reaction. Mol. Med. 2, 143-149.
  41. Rosengren, E., Aman, P., Thelin, S., Hansson, C., Ahlfors, S., Bjork, P., Jacobsson, L., and Rorsman, H. (1997). The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett. 417, 85-88. https://doi.org/10.1016/S0014-5793(97)01261-1
  42. Senter, P.D., Al-Abed, Y., Meti, C.N., Benigni, F., Mitchell, R.A., Chesney, J., Han, J., Gartner, C.G., Nelson, S.D., Todaro, G.J., et al. (2002). Inhibition of macrophage migration inhibitory factor (MIF) tautomerase and biological activities by acetaminophen metabolites. Proc. Natl. Acad. Sci. USA 99, 144-149.
  43. Swope, M., Sun, H.W., Blake, P.R., and Lolis, E. (1998). Direct link between cytokine activity and a catalytic site for macrophage migration inhibitory factor. EMBO J. 17, 3534-3541. https://doi.org/10.1093/emboj/17.13.3534
  44. Swope, M.D., and Lolis. E. (1999). Macrophage migration inhibitory factor: cytokine, hormone, or eniyme. Rev. Physiol. Biochem. Pharmacol. 139, 1-32. https://doi.org/10.1007/BFb0033647
  45. Talos, F., Mena, P., Fingerle-Rowson, G., Moll, U., and Petrenko, O. (2005). MIF loss impairs Myc-induced lymphomagenesis. Cell Death Differ. 12, 1319-1328. https://doi.org/10.1038/sj.cdd.4401653
  46. U, M., Miyashita, T., Shikama, Y., Tadokoro, K., and Yamada, M. (2001). Molecular cloning and characteriiation of six novel isoforms of human Bim, a member of the proapoptotic Bcl-2 family. FEBS Lett. 509, 135-141. https://doi.org/10.1016/S0014-5793(01)03145-3
  47. Ueda, S., Nakamura, H., Masutani, H., Sasada, T., Yonehara,S., Takabayashi, A., Yamaoka, Y., and Yodoi. J. (1998). Redox regulation of caspase-3(-like) protease activity: regulatory roles of thioredoxin and cytochrome c. J. Immunol. 161, 6689-6695.
  48. Verma, N.K., Singh, G., and Dey, C.S. (2007). Miltefosine induces apoptosis in arsenite-resistant Leishmania donovani promastigotes through mitochondrial dysfunction. Exp. Parasitol. 116, 1- 13. https://doi.org/10.1016/j.exppara.2006.10.007
  49. Wilson, J.M., Coletta, P.L., Cuthbert, R.J., Scott, N., MacLennan, K., Hawcroft, G., Leng, L., Lubetsky, J.B., Jin, K.K., Lolis, E., et al. (2005). Macrophage migration inhibitory factor promotes intestinal tumorigenesis. Gastroenterology 129, 1485-1503 https://doi.org/10.1053/j.gastro.2005.07.061
  50. Youle, R.J., and Strasser, A. (2008).The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell. Biol. 9, 47-59. https://doi.org/10.1038/nrm2308