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Emerging Roles of an Innate Immune Regulator TAPE in the Toll-Like Receptor and RIG-I-Like Receptor Pathways

  • Kuan-Ru Chen
  • Pin Ling

Abstract

Inflammation alerts the mammalian immune system to defend pathogen invasion or to resolve tissue damage. Dysregulation of inflammation contributes to the development of infectious diseases or inflammation-mediated chronic diseases such as obesity, diabetes, atherosclerosis, and cancer. Pattern-recognition receptors (PRRs) and their downstream regulators in the innate immune system function to trigger inflammation upon sensing molecular components from invading pathogens or damaged host cells. Better understanding of the regulation of PRR-mediated inflammation provides critical insights toward developing the treatment of infectious diseases and chronic inflammatory diseases. However, signaling networks underlying these PRR pathways still remain complicated and have much to be explored. Emerging evidence indicates that subcellular compartments or lipid organelles function as signaling platforms for conveying PRR signaling. Several cellular mediators of these subcellular organelles and vesicle trafficking have emerged to regulate the PPR pathways. In this review, we first highlight recent advances in the cell biology aspects of the Toll-like receptor (TLR) and cytosolic retinoic acid-inducible gene (RIG)-I-like receptor (RLR) pathways. We then focus on discussing a recently identified innate immune regulator called TBK1-associated protein in the endolysosomes (TAPE), also known as CC2D1A/Freud-1/Aki-1. TAPE is an endolysosomal adaptor shown to regulate the endosomal TLR3 and TLR4 pathways and the cytosolic RIG-I and melanoma differentiation-associated gene (MDA)-5 pathways at an early stage.

Keywords

Innate immunity TLR RIG-I MDA5 TAPE 

References

  1. Al-Tawashi A, Jung SY, Liu D, Su B, Qin J (2012) Protein implicated in nonsyndromic mental retardation regulates protein kinase A (PKA) activity. J Biol Chem 287(18):14644–14658. doi: 10.1074/jbc.M111.261875 CrossRefPubMedCentralPubMedGoogle Scholar
  2. Barton GM, Kagan JC (2009) A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat Rev Immunol 9(8):535–542. doi: 10.1038/nri2587 CrossRefPubMedCentralPubMedGoogle Scholar
  3. Blasius AL, Arnold CN, Georgel P, Rutschmann S, Xia Y, Lin P, Ross C, Li X, Smart NG, Beutler B (2010) Slc15a4, AP-3, and Hermansky-Pudlak syndrome proteins are required for Toll-like receptor signaling in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 107(46):19973–19978. doi: 10.1073/pnas.1014051107 CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bozym RA, Delorme-Axford E, Harris K, Morosky S, Ikizler M, Dermody TS, Sarkar SN, Coyne CB (2012) Focal adhesion kinase is a component of antiviral RIG-I-like receptor signaling. Cell Host Microbe 11(2):153–166. doi: 10.1016/j.chom.2012.01.008 CrossRefPubMedCentralPubMedGoogle Scholar
  5. Broz P, Monack DM (2013) Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13(8):551–565. doi: 10.1038/nri3479 CrossRefPubMedGoogle Scholar
  6. Casrouge A, Zhang SY, Eidenschenk C, Jouanguy E, Puel A, Yang K, Alcais A, Picard C, Mahfoufi N, Nicolas N, Lorenzo L, Plancoulaine S, Senechal B, Geissmann F, Tabeta K, Hoebe K, Du X, Miller RL, Heron B, Mignot C, de Villemeur TB, Lebon P, Dulac O, Rozenberg F, Beutler B, Tardieu M, Abel L, Casanova JL (2006) Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314(5797):308–312. doi: 10.1126/science.1128346 CrossRefPubMedGoogle Scholar
  7. Chang CH, Lai LC, Cheng HC, Chen KR, Syue YZ, Lu HC, Lin WY, Chen SH, Huang HS, Shiau AL, Lei HY, Qin J, Ling P (2011) TBK1-associated protein in endolysosomes (TAPE) is an innate immune regulator modulating the TLR3 and TLR4 signaling pathways. J Biol Chem 286(9):7043–7051. doi: 10.1074/jbc.M110.164632 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Chen KR, Chang CH, Huang CY, Lin CY, Lin WY, Lo YC, Yang CY, Hsing EW, Chen LF, Shih SR, Shiau AL, Lei HY, Tan TH, Ling P (2012) TBK1-associated protein in endolysosomes (TAPE)/CC2D1A is a key regulator linking RIG-I-like receptors to antiviral immunity. J Biol Chem 287(38):32216–32221. doi: 10.1074/jbc.C112.394346 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Chiang HS, Zhao Y, Song JH, Liu S, Wang N, Terhorst C, Sharpe AH, Basavappa M, Jeffrey KL, Reinecker HC (2014) GEF-H1 controls microtubule-dependent sensing of nucleic acids for antiviral host defenses. Nat Immunol 15(1):63–71. doi: 10.1038/ni.2766 CrossRefPubMedCentralPubMedGoogle Scholar
  10. Childress JL, Acar M, Tao C, Halder G (2006) Lethal giant discs, a novel C2-domain protein, restricts notch activation during endocytosis. Curr Biol 16(22):2228–2233. doi: 10.1016/j.cub.2006.09.031 CrossRefPubMedCentralPubMedGoogle Scholar
  11. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, Nagel WE, Fava E, Kalaidzidis Y, Zerial M (2010) Systems survey of endocytosis by multiparametric image analysis. Nature 464(7286):243–249. doi: 10.1038/nature08779 CrossRefPubMedGoogle Scholar
  12. Fukui R, Saitoh S, Kanno A, Onji M, Shibata T, Ito A, Matsumoto M, Akira S, Yoshida N, Miyake K (2011) Unc93B1 restricts systemic lethal inflammation by orchestrating Toll-like receptor 7 and 9 trafficking. Immunity 35(1):69–81. doi: 10.1016/j.immuni.2011.05.010 CrossRefPubMedGoogle Scholar
  13. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446(7138):916–920. doi: 10.1038/nature05732 CrossRefPubMedGoogle Scholar
  14. Gallagher CM, Knoblich JA (2006) The conserved c2 domain protein lethal (2) giant discs regulates protein trafficking in Drosophila. Dev Cell 11(5):641–653. doi: 10.1016/j.devcel.2006.09.014 CrossRefPubMedGoogle Scholar
  15. Gillingham AK, Munro S (2003) Long coiled-coil proteins and membrane traffic. Biochim Biophys Acta 1641(2–3):71–85CrossRefPubMedGoogle Scholar
  16. Goubau D, Deddouche S, Reis ESC (2013) Cytosolic sensing of viruses. Immunity 38(5):855–869. doi: 10.1016/j.immuni.2013.05.007 CrossRefPubMedGoogle Scholar
  17. Hacker H, Karin M (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006(357):re13. doi: 10.1126/stke.3572006re13 CrossRefPubMedGoogle Scholar
  18. Huang J, Liu T, Xu LG, Chen D, Zhai Z, Shu HB (2005) SIKE is an IKK epsilon/TBK1-associated suppressor of TLR3- and virus-triggered IRF-3 activation pathways. EMBO J 24(23):4018–4028CrossRefPubMedCentralPubMedGoogle Scholar
  19. Hurley JH, Hanson PI (2010) Membrane budding and scission by the ESCRT machinery: it’s all in the neck. Nat Rev Mol Cell Biol 11(8):556–566. doi: 10.1038/nrm2937 CrossRefPubMedCentralPubMedGoogle Scholar
  20. Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327(5963):291–295. doi: 10.1126/science.1183021 CrossRefPubMedCentralPubMedGoogle Scholar
  21. Jaekel R, Klein T (2006) The Drosophila Notch inhibitor and tumor suppressor gene lethal (2) giant discs encodes a conserved regulator of endosomal trafficking. Dev Cell 11(5):655–669. doi: 10.1016/j.devcel.2006.09.019 CrossRefPubMedGoogle Scholar
  22. Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13CrossRefPubMedGoogle Scholar
  23. Jiang X, Kinch LN, Brautigam CA, Chen X, Du F, Grishin NV, Chen ZJ (2012) Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 36(6):959–973. doi: 10.1016/j.immuni.2012.03.022 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Jung SY, Malovannaya A, Wei J, O’Malley BW, Qin J (2005) Proteomic analysis of steady-state nuclear hormone receptor coactivator complexes. Mol Endocrinol 19(10):2451–2465CrossRefPubMedGoogle Scholar
  25. Kagan JC (2012) Signaling organelles of the innate immune system. Cell 151(6):1168–1178. doi: 10.1016/j.cell.2012.11.011 CrossRefPubMedCentralPubMedGoogle Scholar
  26. Kawagoe T, Takeuchi O, Takabatake Y, Kato H, Isaka Y, Tsujimura T, Akira S (2009) TANK is a negative regulator of Toll-like receptor signaling and is critical for the prevention of autoimmune nephritis. Nat Immunol 10(9):965–972CrossRefPubMedCentralPubMedGoogle Scholar
  27. Kim YM, Brinkmann MM, Paquet ME, Ploegh HL (2008) UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452(7184):234–238. doi: 10.1038/nature06726 CrossRefPubMedGoogle Scholar
  28. Koshiba T, Yasukawa K, Yanagi Y, Kawabata S (2011) Mitochondrial membrane potential is required for MAVS-mediated antiviral signaling. Sci Signal 4(158):ra7. doi: 10.1126/scisignal.2001147
  29. Lee BL, Moon JE, Shu JH, Yuan L, Newman ZR, Schekman R, Barton GM (2013) UNC93B1 mediates differential trafficking of endosomal TLRs. Elife 2:e00291. doi: 10.7554/eLife.00291 PubMedCentralPubMedGoogle Scholar
  30. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9(2):99–111CrossRefPubMedGoogle Scholar
  31. Loo YM, Gale M Jr (2011) Immune signaling by RIG-I-like receptors. Immunity 34(5):680–692. doi: 10.1016/j.immuni.2011.05.003 CrossRefPubMedCentralPubMedGoogle Scholar
  32. Martinelli N, Hartlieb B, Usami Y, Sabin C, Dordor A, Miguet N, Avilov SV, Ribeiro EA Jr, Gottlinger H, Weissenhorn W (2012) CC2D1A is a regulator of ESCRT-III CHMP4B. J Mol Biol 419(1–2):75–88. doi: 10.1016/j.jmb.2012.02.044 CrossRefPubMedCentralPubMedGoogle Scholar
  33. Matsuda A, Suzuki Y, Honda G, Muramatsu S, Matsuzaki O, Nagano Y, Doi T, Shimotohno K, Harada T, Nishida E, Hayashi H, Sugano S (2003) Large-scale identification and characterization of human genes that activate NF-kappaB and MAPK signaling pathways. Oncogene 22(21):3307–3318CrossRefPubMedGoogle Scholar
  34. Nakamura A, Naito M, Tsuruo T, Fujita N (2008) Freud-1/Aki1, a novel PDK1-interacting protein, functions as a scaffold to activate the PDK1/Akt pathway in epidermal growth factor signaling. Mol Cell Biol 28(19):5996–6009. doi: 10.1128/MCB. 00114-08 CrossRefPubMedCentralPubMedGoogle Scholar
  35. O’Neill LA, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7(5):353–364. doi: 10.1038/nri2079 CrossRefPubMedGoogle Scholar
  36. Oshiumi H, Miyashita M, Inoue N, Okabe M, Matsumoto M, Seya T (2010) The ubiquitin ligase Riplet is essential for RIG-I-dependent innate immune responses to RNA virus infection. Cell Host Microbe 8(6):496–509. doi: 10.1016/j.chom.2010.11.008 CrossRefPubMedGoogle Scholar
  37. Paludan SR, Bowie AG (2013) Immune sensing of DNA. Immunity 38(5):870–880. doi: 10.1016/j.immuni.2013.05.004 CrossRefPubMedCentralPubMedGoogle Scholar
  38. Rogaeva A, Albert PR (2007) The mental retardation gene CC2D1A/Freud-1 encodes a long isoform that binds conserved DNA elements to repress gene transcription. Eur J Neurosci 26(4):965–974. doi: 10.1111/j.1460-9568.2007.05727.x CrossRefPubMedGoogle Scholar
  39. Ryzhakov G, Randow F (2007) SINTBAD, a novel component of innate antiviral immunity, shares a TBK1-binding domain with NAP1 and TANK. EMBO J 26(13):3180–3190CrossRefPubMedCentralPubMedGoogle Scholar
  40. Sasai M, Shingai M, Funami K, Yoneyama M, Fujita T, Matsumoto M, Seya T (2006) NAK-associated protein 1 participates in both the TLR3 and the cytoplasmic pathways in type I IFN induction. J Immunol 177(12):8676–8683CrossRefPubMedGoogle Scholar
  41. Sasai M, Linehan MM, Iwasaki A (2010) Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 329(5998):1530–1534. doi: 10.1126/science.1187029 CrossRefPubMedCentralPubMedGoogle Scholar
  42. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820. doi: 10.1016/j.cell.2010.01.022 CrossRefPubMedGoogle Scholar
  43. Troost T, Jaeckel S, Ohlenhard N, Klein T (2012) The tumour suppressor Lethal (2) giant discs is required for the function of the ESCRT-III component Shrub/CHMP4. J Cell Sci 125(Pt 3):763–776. doi: 10.1242/jcs.097261 CrossRefPubMedGoogle Scholar
  44. Usami Y, Popov S, Weiss ER, Vriesema-Magnuson C, Calistri A, Gottlinger HG (2012) Regulation of CHMP4/ESCRT-III function in human immunodeficiency virus type 1 budding by CC2D1A. J Virol 86(7):3746–3756. doi: 10.1128/JVI. 06539-11 CrossRefPubMedCentralPubMedGoogle Scholar
  45. Zeng W, Sun L, Jiang X, Chen X, Hou F, Adhikari A, Xu M, Chen ZJ (2010) Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell 141(2):315–330. doi: 10.1016/j.cell.2010.03.029 CrossRefPubMedCentralPubMedGoogle Scholar
  46. Zhao M, Li XD, Chen Z (2010) CC2D1A, a DM14 and C2 domain protein, activates NF-kappaB through the canonical pathway. J Biol Chem 285(32):24372–24380. doi: 10.1074/jbc.M109.100057 CrossRefPubMedCentralPubMedGoogle Scholar
  47. Zhao M, Raingo J, Chen ZJ, Kavalali ET (2011) Cc2d1a, a C2 domain containing protein linked to nonsyndromic mental retardation, controls functional maturation of central synapses. J Neurophysiol 105(4):1506–1515. doi: 10.1152/jn.00950.2010 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  1. 1.Institute of Basic Medical Sciences, College of MedicineNational Cheng Kung UniversityTainanTaiwan
  2. 2.Department of Microbiology and Immunology, College of MedicineNational Cheng Kung UniversityTainanTaiwan
  3. 3.Department of Medical Laboratory Science and Biotechnology, College of MedicineNational Cheng Kung UniversityTainanTaiwan
  4. 4.Center of Infectious Disease and Signaling Research, College of Medicine, National ChengKung UniversityTainanTaiwan

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