The roles of Pellino E3 ubiquitin ligases in immunity

Nature Reviews Immunology

Volumn 14, Issue 2, 2014, Pages 122-131

  Moynagh, Paul N ^a,b  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; HISTIDINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; PELLINO 2 PROTEIN; PELLINO 3 PROTEIN; PELLINO PROTEIN; PHOSPHOTHREONINE; SMAD6 PROTEIN; SMAD7 PROTEIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; CELL STRAIN HEK293; CHRONIC OBSTRUCTIVE LUNG DISEASE; CRYSTAL STRUCTURE; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; IMMUNITY; INNATE IMMUNITY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; T LYMPHOCYTE; UBIQUITINATION;

ANIMALS; HUMANS; IMMUNITY, INNATE; NOD2 SIGNALING ADAPTOR PROTEIN; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84893637996     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3599     Document Type: Review

References (62)

1. O'Neill, L. A., Golenbock, D. and Bowie, A. G. The history of Toll-like receptors - redefining innate immunity. Nature Rev. Immunol. 13, 453-460 (2013).
2. Chen, G., Shaw, M. H., Kim, Y. G. and Nunez, G. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 4, 365-398 (2009).
3. Loo, Y. M. and Gale, M. Jr. Immune signaling by RIG-I-like receptors. Immunity 34, 680-692 (2011).
4. Paludan, S. R. and Bowie, A. G. Immune sensing of DNA. Immunity 38, 870-880 (2013).
5. Jiang, X. and Chen, Z. J. The role of ubiquitylation in immune defence and pathogen evasion. Nature Rev. Immunol. 12, 35-48 (2012).
6. Grosshans, J., Schnorrer, F. and Nüsslein-Volhard, C. Oligomerisation of Tube and Pelle leads to nuclear localisation of dorsal. Mech. Dev. 81, 127-138 (1999).
7. Haghayeghi, A., Sarac, A., Czerniecki, S., Grosshans, J. and Schock, F. Pellino enhances innate immunity in Drosophila. Mech. Dev. 127, 301-307 (2010).
8. Yu, K. Y. et al. Cutting edge: mouse Pellino-2 modulates IL-1 and lipopolysaccharide signaling. J. Immunol. 169, 4075-4078 (2002).
9. Jiang, Z. et al. Pellino 1 is required for interleukin-1 (IL-1)-mediated signaling through its interaction with the IL-1 receptor-associated kinase 4 (IRAK4)-IRAK-tumor necrosis factor receptor-associated factor 6 (TRAF6) complex. J. Biol. Chem. 278, 10952-10956 (2003).
10. Jensen, L. E. and Whitehead, A. S. Pellino3, a novel member of the Pellino protein family, promotes activation of c-Jun and Elk-1 and may act as a scaffolding protein. J. Immunol. 171, 1500-1506 (2003).
11. Rich, T., Allen, R. L., Lucas, A. M., Stewart, A. and Trowsdale, J. Pellino-related sequences from Caenorhabditis elegans and Homo sapiens. Immunogenetics 52, 145-149 (2000).
12. Resch, K., Jockusch, H. and Schmitt-John, T. Assignment of homologous genes, Peli1/PELI1 and Peli2/PELI2, for the Pelle adaptor protein Pellino to mouse chromosomes 11 and 14 and human chromosomes 2p13.3 and 14q21, respectively, by physical and radiation hybrid mapping. Cytogenet. Cell Genet. 92, 172-174 (2001).
13. Schauvliege, R., Janssens, S. and Beyaert, R. Pellino proteins are more than scaffold proteins in TLR/IL-1R signalling: a role as novel RING E3-ubiquitin-ligases. FEBS Lett. 580, 4697-4702 (2006).
14. Strelow, A., Kollewe, C. and Wesche, H. Characterization of Pellino2, a substrate of IRAK1 and IRAK4. FEBS Lett. 547, 157-161 (2003).
15. Jensen, L. E. and Whitehead, A. S. Pellino2 activates the mitogen activated protein kinase pathway. FEBS Lett. 545, 199-202 (2003).
16. Butler, M. P., Hanly, J. A. and Moynagh, P. N. Pellino3 is a novel upstream regulator of p38 MAPK and activates CREB in a p38-dependent manner. J. Biol. Chem. 280, 27759-27768 (2005).
17. Butler, M. P., Hanly, J. A. and Moynagh, P. N. Kinase-active interleukin-1 receptor-associated kinases promote polyubiquitination and degradation of the Pellino family: direct evidence for PELLINO proteins being ubiquitin-protein isopeptide ligases. J. Biol. Chem. 282, 29729-29737 (2007).
18. Ordureau, A. et al. The IRAK-catalysed activation of the E3 ligase function of Pellino isoforms induces the Lys63-linked polyubiquitination of IRAK1. Biochem. J. 409, 43-52 (2008).
19. Lin, C. C., Huoh, Y. S., Schmitz, K. R., Jensen, L. E. and Ferguson, K. M. Pellino proteins contain a cryptic FHA domain that mediates interaction with phosphorylated IRAK1. Structure 16, 1806-1816 (2008).
20. Smith, H. et al. Identification of the phosphorylation sites on the E3 ubiquitin ligase Pellino that are critical for activation by IRAK1 and IRAK4. Proc. Natl Acad. Sci. USA 106, 4584-4590 (2009).
21. Smith, H. et al. The role of TBK1 and IKKε in the expression and activation of Pellino 1. Biochem. J. 434, 537-548 (2011).
22. Goh, E. T. et al. Identification of the protein kinases that activate the E3 ubiquitin ligase Pellino 1 in the innate immune system. Biochem. J. 441, 339-346 (2012).
23. Baines, K. J. et al. Novel immune genes associated with excessive inflammatory and antiviral responses to rhinovirus in COPD. Respir. Res. 14, 15 (2013).
24. Bennett, J. A. et al. Pellino-1 selectively regulates epithelial cell responses to rhinovirus. J. Virol. 86, 6595-6604 (2012).
25. Baines, K. J., Simpson, J. L., Wood, L. G., Scott, R. J. and Gibson, P. G. Transcriptional phenotypes of asthma defined by gene expression profiling of induced sputum samples. J. Allergy Clin. Immunol. 127, 153-160 (2011).
26. Kim, J. H. et al. Pellino-1, an adaptor protein of interleukin-1 receptor/toll-like receptor signaling, is sumoylated by Ubc9. Mol. Cells 31, 85-89 (2011).
27. Choi, K. C. et al. Smad6 negatively regulates interleukin 1-receptor-Toll-like receptor signaling through direct interaction with the adaptor Pellino-1. Nature Immunol. 7, 1057-1065 (2006).
28. Lee, Y. S. et al. Smad7 and Smad6 bind to discrete regions of Pellino-1 via their MH2 domains to mediate TGF-β1-induced negative regulation of IL-1R/TLR signaling. Biochem. Biophys. Res. Commun. 393, 836-843 (2010).
29. Kim, T. W. et al. Pellino 2 is critical for Toll-like receptor/interleukin-1 receptor (TLR/IL-1R)-mediated post-transcriptional control. J. Biol. Chem. 287, 25686-25695 (2012).
30. Chang, M., Jin, W. and Sun, S. C. Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nature Immunol. 10, 1089-1095 (2009).
31. Cusson-Hermance, N., Khurana, S., Lee, T. H., Fitzgerald, K. A. and Kelliher, M. A. Rip1 mediates the Trif-dependent toll-like receptor 3- and 4-induced NF-κB activation but does not contribute to interferon regulatory factor 3 activation. J. Biol. Chem. 280, 36560-36566 (2005).
32. Yamamoto, M. et al. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFNβ promoter in the Toll-like receptor signaling. J. Immunol. 169, 6668-6672 (2002).
33. Oshiumi, H., Matsumoto, M., Funami, K., Akazawa, T. and Seya, T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nature Immunol. 4, 161-167 (2003).
34. Yamamoto, M. et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643 (2003).
35. Fitzgerald, K. A. et al. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nature Immunol. 4, 491-496 (2003).
36. Sharma, S. et al. Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151 (2003).
37. Enesa, K. et al. Pellino1 is required for interferon production by viral double-stranded RNA. J. Biol. Chem. 287, 34825-34835 (2012).
38. Ordureau, A. et al. DEAF1 is a Pellino1-interacting protein required for interferon production by Sendai virus and double-stranded RNA. J. Biol. Chem. 288, 24569-24580 (2013).
39. Xiao, Y. et al. Peli1 promotes microglia-mediated CNS inflammation by regulating Traf3 degradation. Nature Med. 19, 595-602 (2013).
40. Tseng, P. H. et al. Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nature Immunol. 11, 70-75 (2010).
41. Chang, M. et al. The ubiquitin ligase Peli1 negatively regulates T cell activation and prevents autoimmunity. Nature Immunol. 12, 1002-1009 (2011).
42. Moynagh, P. N. Peli1 (rel)ieves autoimmunity. Nature Immunol. 12, 927-929 (2011).
43. Liu, Y. et al. BCL10 mediates lipopolysaccharide/ toll-like receptor-4 signaling through interaction with Pellino2. J. Biol. Chem. 279, 37436-37444 (2004).
44. Xiao, H. et al. Pellino 3b negatively regulates interleukin-1-induced TAK1-dependent NF-κB activation. J. Biol. Chem. 283, 14654-14664 (2008).
45. Mellett, M., Atzei, P., Jackson, R., O'Neill, L. A. and Moynagh, P. N. Mal mediates TLR-induced activation of CREB and expression of IL-10. J. Immunol. 186, 4925-4935 (2011).
46. Siednienko, J. et al. Pellino3 targets the IRF7 pathway and facilitates autoregulation of TLR3- and viral-induced expression of type I interferons. Nature Immunol. 13, 1055-1062 (2012).
47. Ning, S., Campos, A. D., Darnay, B. G., Bentz, G. L. and Pagano, J. S. TRAF6 and the three C-terminal lysine sites on IRF7 are required for its ubiquitination-mediated activation by the tumor necrosis factor receptor family member latent membrane protein 1. Mol. Cell. Biol. 28, 6536-6546 (2008).
48. Tzieply, N. et al. OxLDL inhibits LPS-induced IFNβ expression by Pellino3- and IRAK1/4-dependent modification of TANK. Cell Signal. 24, 1141-1149 (2012).
49. Conway, J. P. and Kinter, M. Proteomic and transcriptomic analyses of macrophages with an increased resistance to oxidized low density lipoprotein (oxLDL)-induced cytotoxicity generated by chronic exposure to oxLDL. Mol. Cell Proteom. 4, 1522-1540 (2005).
50. Yang, S. et al. Pellino3 ubiquitinates RIP2 and mediates Nod2-induced signaling and protective effects in colitis. Nature Immunol. 14, 927-936 (2013).
51. Rubino, S. J., Selvanantham, T., Girardin, S. E. and Philpott, D. J. Nod-like receptors in the control of intestinal inflammation. Curr. Opin. Immunol. 24, 398-404 (2012).
52. Damgaard, R. B. et al. The ubiquitin ligase XIAP recruits LUBAC for NOD2 signaling in inflammation and innate immunity. Mol. Cell 46, 746-758 (2012).
53. Emmerich, C. H. et al. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc. Natl Acad. Sci. USA 110, 15247-15252 (2013).
54. Yang, S. et al. Pellino3 targets RIP1 and regulates the pro-apoptotic effects of TNFα. Nature Commun. 4, 2583 (2013).
55. Aggarwal, B. B. Signalling pathways of the TNF superfamily: a double-edged sword. Nature Rev. Immunol. 3, 745-756 (2003).
56. Wong, W. W. et al. RIPK1 is not essential for TNFR1-induced activation of NF-κB. Cell Death Differ. 17, 482-487 (2010).
57. Griffin, B. D. et al. A poxviral homolog of the Pellino protein inhibits Toll and Toll-like receptor signalling. Eur. J. Immunol. 41, 798-812 (2011).
58. Nogueira, E. et al. Toll-like receptors-related genes in kidney transplant patients with chronic allograft nephropathy and acute rejection. Int. Immunopharmacol. 9, 673-676 (2009).
59. Kim, J. J. et al. Assessment of risk factors for Korean children with Kawasaki disease. Pediatr. Cardiol. 33, 513-520 (2012).
60. Kim, J. J. et al. A genome-wide association analysis reveals 1p31 and 2p13.3 as susceptibility loci for Kawasaki disease. Hum. Genet. 129, 487-495 (2011).
61. Malynn, B. A. and Ma, A. Ubiquitin makes its mark on immune regulation. Immunity 33, 843-852 (2010).
62. Kirisako, T. et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J. 25, 4877-4887 (2006).