Regulation of RIPK1 activation by TAK1-mediated phosphorylation dictates apoptosis and necroptosis

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Geng, Jiefei ^a   Ito, Yasushi ^a   Shi, Linyu ^b   Amin, Palak ^a   Chu, Jiachen ^a   Ouchida, Amanda Tomie ^a   Mookhtiar, Adnan Kasim ^a   Zhao, Heng ^a   Xu, Daichao ^a   Shan, Bing ^b   Najafov, Ayaz ^a   Gao, Guangping ^c   Akira, Shizuo ^d   Yuan, Junying ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOHEXIMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN DERIVATIVE; PROTEIN RIPK1; SERINE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR RECEPTOR 1;

APOPTOSIS; BIOCHEMISTRY; BIOMARKER; CELLS AND CELL COMPONENTS; CYTOGENETICS; ENZYME; INHIBITION; PHYSIOLOGICAL RESPONSE; PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NECROPTOSIS; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL DEATH; CHEMISTRY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CELL DEATH; CELLS, CULTURED; CYCLOHEXIMIDE; MAP KINASE KINASE KINASES; MICE; NF-KAPPA B; PHOSPHORYLATION; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85028411517     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00406-w     Document Type: Article

References (34)

1. Ofengeim, D. & Yuan, J. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 14, 727-736 (2013).
2. Wallach, D., Kang, T. B., Dillon, C. P. & Green, D. R. Programmed necrosis in inflammation: toward identification of the effector molecules. Science 352, aaf2154 (2016).
3. Kanayama, A. et al. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535-548 (2004).
4. Wang, C. et al. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 412, 346-351 (2001).
5. Dondelinger, Y. et al. NF-kappaB-independent role of IKKalpha/IKKbeta in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol. Cell 60, 63-76 (2015).
6. Mihaly, S. R., Ninomiya-Tsuji, J. & Morioka, S. TAK1 control of cell death. Cell. Death Differ. 21, 1667-1676 (2014).
7. Onizawa, M. et al. The ubiquitin-modifying enzyme A20 restricts ubiquitination of the kinase RIPK3 and protects cells from necroptosis. Nat. Immunol. 16, 618-627 (2015).
8. Morioka, S. et al. TAK1 kinase switches cell fate from apoptosis to necrosis following TNF stimulation. J. Cell Biol. 204, 607-623 (2014).
9. Zhou, W. & Yuan, J. Necroptosis in health and diseases. Semin. Cell Dev. Biol. 35, 14-23 (2014).
10. Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112-119 (2005).
11. Degterev, A. et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4, 313-321 (2008).
12. Huttlin, E. L. et al. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189 (2010).
13. Zhang, J., Clark, K., Lawrence, T., Peggie, M. W. & Cohen, P. An unexpected twist to the activation of IKKbeta: TAK1 primes IKKbeta for activation by autophosphorylation. Biochem. J. 461, 531-537 (2014).
14. Sato, S. et al. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6, 1087-1095 (2005).
15. Moriguchi, T. et al. A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3. J. Biol. Chem. 271, 13675-13679 (1996).
16. Broglie, P., Matsumoto, K., Akira, S., Brautigan, D. L. & Ninomiya-Tsuji, J. Transforming growth factor beta-activated kinase 1 (TAK1) kinase adaptor, TAK1-binding protein 2, plays dual roles in TAK1 signaling by recruiting both an activator and an inhibitor of TAK1 kinase in tumor necrosis factor signaling pathway. J. Biol. Chem. 285, 2333-2339 (2010).
17. Delhase, M., Hayakawa, M., Chen, Y. & Karin, M. Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science 284, 309-313 (1999).
18. Ea, C. K., Deng, L., Xia, Z. P., Pineda, G. & Chen, Z. J. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22, 245-257 (2006).
19. Lu, J. et al. SM-164: a novel, bivalent Smac mimetic that induces apoptosis and tumor regression by concurrent removal of the blockade of cIAP-1/2 and XIAP. Cancer Res. 68, 9384-9393 (2008).
20. Pobezinskaya, Y. L. et al. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 9, 1047-1054 (2008).
21. Wertz, I. E. et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature. 430, 694-699 (2004).
22. Newton, K. et al. RIPK3 deficiency or catalytically inactive RIPK1 provides greater benefit than MLKL deficiency in mouse models of inflammation and tissue injury. Cell Death Differ. 23, 1565-1576 (2016).
23. Gao, K. et al. Empty virions in AAV8 vector preparations reduce transduction efficiency and may cause total viral particle dose-limiting side-effects. Mol. Ther. Methods Clin. Dev. 1, 20139 (2014).
24. Yan, Z., Yan, H. & Ou, H. Human thyroxine binding globulin (TBG) promoter directs efficient and sustaining transgene expression in liver-specific pattern. Gene 506, 289-294 (2012).
25. Lin, Y., Devin, A., Rodriguez, Y. & Liu, Z. G. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13, 2514-2526 (1999).
26. Ofengeim, D. et al. Activation of necroptosis in multiple sclerosis. Cell Rep. 10, 1836-1849 (2015).
27. Berger, S. B. et al. Cutting edge: RIP1 kinase activity is dispensable for normal development but is a key regulator of inflammation in SHARPIN-deficient mice. J. Immunol. 192, 5476-5480 (2014).
28. Blonska, M. et al. TAK1 is recruited to the tumor necrosis factor-alpha (TNFalpha) receptor 1 complex in a receptor-interacting protein (RIP)-dependent manner and cooperates with MEKK3 leading to NF-kappaB activation. J. Biol. Chem. 280, 43056-43063 (2005).
29. Hayden, M. S. & Ghosh, S. Shared principles in NF-kappaB signaling. Cell 132, 344-362 (2008).
30. Song, H. Y., Rothe, M. & Goeddel, D. V. The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc. Natl Acad. Sci. USA 93, 6721-6725 (1996).
31. Wertz, I. E. et al. Phosphorylation and linear ubiquitin direct A20 inhibition of inflammation. Nature 528, 370-375 (2015).
32. Mele, A., Cervantes, J. R., Chien, V., Friedman, D. & Ferran, C. Single nucleotide polymorphisms at the TNFAIP3/A20 locus and susceptibility/ resistance to inflammatory and autoimmune diseases. Adv. Exp. Med. Biol. 809, 163-183 (2014).
33. Mueller, C., Ratner, D., Zhong, L., Esteves-Sena, M. & Gao, G. Production and discovery of novel recombinant adeno-associated viral vectors. Curr. Protoc. Microbiol. 26, 14D.1.1-14D.1.21 (2012).
34. Cryns, V. L., Bergeron, L., Zhu, H., Li, H. & Yuan, J. Specific cleavage of alphafodrin during Fas-and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1beta-converting enzyme/Ced-3 protease distinct from the poly (ADP-ribose) polymerase protease. J. Biol. Chem. 271, 31277-31282 (1996).