Optineurin Regulates the Interferon Response in a Cell Cycle-Dependent Manner

1. Ivashkiv LB, Donlin LT (2014) Regulation of type I interferon responses. Nat Rev Immunol 14 : 36–49. doi: 10.1038/nri3581 24362405

2. Schneider WM, Chevillotte MD, Rice CM (2014) Interferon-stimulated genes: a complex web of host defenses. Ann Rev Immunol 32 : 513–545. doi: 10.1146/annurev-immunol-032713-120231 24555472

3. Wu J, Chen ZJ (2014) Innate immune sensing and signaling of cytosolic nucleic acids. Ann Rev Immunol 32 : 461–488. doi: 10.1146/annurev-immunol-032713-120156 24655297

4. Chiu YH, Macmillan JB, Chen ZJ (2009) RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138 : 576–591. doi: 10.1016/j.cell.2009.06.015 19631370

5. Myong S, Cui S, Cornish PV, Kirchhofer A, Gack MU, et al. (2009) Cytosolic viral sensor RIG-I is a 5'-triphosphate-dependent translocase on double-stranded RNA. Science 323 : 1070–1074. doi: 10.1126/science.1168352 19119185

6. Koshiba T (2013) Mitochondrial-mediated antiviral immunity. Biochim Biophys Acta 1833 : 225–232. doi: 10.1016/j.bbamcr.2012.03.005 22440325

7. Jacobs JL, Coyne CB (2013) Mechanisms of MAVS regulation at the mitochondrial membrane. J Mol Biol 425 : 5009–5019. doi: 10.1016/j.jmb.2013.10.007 24120683

8. Hiscott J (2007) Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev 18 : 483–490. 17706453

9. Genin P, Vaccaro A, Civas A (2009) The role of differential expression of human interferon—a genes in antiviral immunity. Cytokine Growth Factor Rev s 20 : 283–295. doi: 10.1016/j.cytogfr.2009.07.005 19651532

10. Chen W, Royer WE Jr. (2010) Structural insights into interferon regulatory factor activation. Cell Signal 22 : 883–887. doi: 10.1016/j.cellsig.2009.12.005 20043992

11. Helgason E, Phung QT, Dueber EC (2013) Recent insights into the complexity of Tank-binding kinase 1 signaling networks: the emerging role of cellular localization in the activation and substrate specificity of TBK1. FEBS lett 587 : 1230–1237. doi: 10.1016/j.febslet.2013.01.059 23395801

12. Li S, Wang L, Berman M, Kong YY, Dorf ME (2011) Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35 : 426–440. doi: 10.1016/j.immuni.2011.06.014 21903422

13. Korac J, Schaeffer V, Kovacevic I, Clement AM, Jungblut B, et al. (2013) Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J Sell Science 126 : 580–592.

14. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, et al. (2011) Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333 : 228–233. doi: 10.1126/science.1205405 21617041

15. Ikeda F, Hecker CM, Rozenknop A, Nordmeier RD, Rogov V, et al. (2007) Involvement of the ubiquitin-like domain of TBK1/IKK-i kinases in regulation of IFN-inducible genes. EMBO J 26 : 3451–3462. 17599067

16. Wang L, Li S, Dorf ME (2012) NEMO binds ubiquitinated TANK-binding kinase 1 (TBK1) to regulate innate immune responses to RNA viruses. PloS one 7: e43756. doi: 10.1371/journal.pone.0043756 23028469

17. Clark K, Takeuchi O, Akira S, Cohen P (2011) The TRAF-associated protein TANK facilitates cross-talk within the IkappaB kinase family during Toll-like receptor signaling. Proc Nat Acad Sciences U.S.A 108 : 17093–17098. doi: 10.1073/pnas.1114194108 21949249

18. Lei CQ, Zhong B, Zhang Y, Zhang J, Wang S, et al. (2010) Glycogen synthase kinase 3beta regulates IRF3 transcription factor-mediated antiviral response via activation of the kinase TBK1. Immunity 33 : 878–889. doi: 10.1016/j.immuni.2010.11.021 21145761

19. Gabhann JN, Higgs R, Brennan K, Thomas W, Damen JE, et al. (2010) Absence of SHIP-1 results in constitutive phosphorylation of tank-binding kinase 1 and enhanced TLR3-dependent IFN-beta production. J Immunol 184 : 2314–2320. doi: 10.4049/jimmunol.0902589 20100929

20. Zhao Y, Liang L, Fan Y, Sun S, An L, et al. (2012) PPM1B negatively regulates antiviral response via dephosphorylating TBK1. Cell Signal 24 : 2197–2204. doi: 10.1016/j.cellsig.2012.06.017 22750291

21. Wang C, Chen T, Zhang J, Yang M, Li N, et al. (2009) The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat Immunol 10 : 744–752. doi: 10.1038/ni.1742 19483718

22. Friedman CS, O'Donnell MA, Legarda-Addison D, Ng A, Cardenas WB, et al. (2008) The tumour suppressor CYLD is a negative regulator of RIG-I-mediated antiviral response. EMBO Rep 9 : 930–936. doi: 10.1038/embor.2008.136 18636086

23. Zhang M, Wu X, Lee AJ, Jin W, Chang M, et al. (2008) Regulation of IkappaB kinase-related kinases and antiviral responses by tumor suppressor CYLD. J Biol Chem 283 : 18621–18626. doi: 10.1074/jbc.M801451200 18467330

24. Parvatiyar K, Barber GN, Harhaj EW (2010) TAX1BP1 and A20 inhibit antiviral signaling by targeting TBK1-IKKi kinases. J Biol Chem 285 : 14999–15009. doi: 10.1074/jbc.M110.109819 20304918

25. Zhang L, Zhao X, Zhang M, Zhao W, Gao C (2014) Ubiquitin-Specific Protease 2b Negatively Regulates IFN-beta Production and Antiviral Activity by Targeting TANK-Binding Kinase 1. J Immunol 193 : 2230–2237. doi: 10.4049/jimmunol.1302634 25070846

26. Charoenthongtrakul S, Gao L, Parvatiyar K, Lee D, Harhaj EW (2013) RING finger protein 11 targets TBK1/IKKi kinases to inhibit antiviral signaling. PloS one 8: e53717. doi: 10.1371/journal.pone.0053717 23308279

27. Belgnaoui SM, Paz S, Samuel S, Goulet ML, Sun Q, et al. (2012) Linear ubiquitination of NEMO negatively regulates the interferon antiviral response through disruption of the MAVS-TRAF3 complex. Cell Host & Microbe 12 : 211–222.

28. Li Y, Kang J, Horwitz MS (1998) Interaction of an adenovirus E3 14.7-kilodalton protein with a novel tumor necrosis factor alpha-inducible cellular protein containing leucine zipper domains. Mol Cell Biol 18 : 1601–1610. 9488477

29. Schwamborn K, Weil R, Courtois G, Whiteside ST, Israel A (2000) Phorbol esters and cytokines regulate the expression of the NEMO-related protein, a molecule involved in a NF-kappa-B-independent pathway. J Biol Chem y 275 : 22780–22789. 10807909

30. Munitic I, Giardino Torchia ML, Meena NP, Zhu G, Li CC, et al. (2013) Optineurin insufficiency impairs IRF3 but not NF-kappaB activation in immune cells. J Immunol 191 : 6231–6240. doi: 10.4049/jimmunol.1301696 24244017

31. Journo C, Filipe J, About F, Chevalier SA, Afonso PV, et al. (2009) NRP/Optineurin Cooperates with TAX1BP1 to potentiate the activation of NF-kappaB by human T-lymphotropic virus type 1 tax protein. PLoS Pathogens 5: e1000521. doi: 10.1371/journal.ppat.1000521 19609363

32. Ying H, Yue BY (2012) Cellular and molecular biology of optineurin. Int Rev Cell Mol Biol 294 : 223–258. doi: 10.1016/B978-0-12-394305-7.00005-7 22364875

33. Kachaner D, Genin P, Laplantine E, Weil R (2012) Toward an integrative view of Optineurin functions. Cell Cycle 11 : 2808–2818. doi: 10.4161/cc.20946 22801549

34. Morton S, Hesson L, Peggie M, Cohen P (2008) Enhanced binding of TBK1 by an optineurin mutant that causes a familial form of primary open angle glaucoma. FEBS lett 582 : 997–1002. doi: 10.1016/j.febslet.2008.02.047 18307994

35. Gleason CE, Ordureau A, Gourlay R, Arthur JS, Cohen P (2011) Polyubiquitin binding to optineurin is required for optimal activation of TANK-binding kinase 1 and production of interferon beta. J Biol Chem 286 : 35663–35674. doi: 10.1074/jbc.M111.267567 21862579

36. Mankouri J, Fragkoudis R, Richards KH, Wetherill LF, Harris M, et al. (2010) Optineurin negatively regulates the induction of IFNbeta in response to RNA virus infection. PLoS Pathogens 6: e1000778. doi: 10.1371/journal.ppat.1000778 20174559

37. Sakaguchi T, Irie T, Kawabata R, Yoshida A, Maruyama H, et al. (2011) Optineurin with amyotrophic lateral sclerosis-related mutations abrogates inhibition of interferon regulatory factor-3 activation. Neuroscience Lett 505 : 279–281. doi: 10.1016/j.neulet.2011.10.040 22040667

38. Kachaner D, Filipe J, Laplantine E, Bauch A, Bennett KL, et al. (2012) Plk1-dependent phosphorylation of optineurin provides a negative feedback mechanism for mitotic progression. Mol Cell 45 : 553–566. doi: 10.1016/j.molcel.2011.12.030 22365832

39. Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, et al. (2010) Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 285 : 10850–10861. doi: 10.1074/jbc.M109.080796 20123989

40. Tu D, Zhu Z, Zhou AY, Yun CH, Lee KE, et al. (2013) Structure and ubiquitination-dependent activation of TANK-binding kinase 1. Cell Rep 3 : 747–758. doi: 10.1016/j.celrep.2013.01.033 23453972

41. Sun SC (2010) CYLD: a tumor suppressor deubiquitinase regulating NF-kappaB activation and diverse biological processes. Cell Death Diff 17 : 25–34.

42. Niu J, Shi Y, Iwai K, Wu ZH (2011) LUBAC regulates NF-kappaB activation upon genotoxic stress by promoting linear ubiquitination of NEMO. EMBO J 30 : 3741–3753. doi: 10.1038/emboj.2011.264 21811235

43. Chalasani ML, Swarup G, Balasubramanian D (2009) Optineurin and its mutants: molecules associated with some forms of glaucoma. Ophthalmic Res 42 : 176–184. doi: 10.1159/000232400 19672125

44. Shembade N, Harhaj EW (2012) Regulation of NF-kappaB signaling by the A20 deubiquitinase. Cell Mol Immunol 9 : 123–130. doi: 10.1038/cmi.2011.59 22343828

45. Kovalenko A, Chable-Bessia C, Cantarella G, Israel A, Wallach D, et al. (2003) The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424 : 801–805. 12917691

46. Nagabhushana A, Bansal M, Swarup G (2011) Optineurin is required for CYLD-dependent inhibition of TNFalpha-induced NF-kappaB activation. PloS one 6: e17477. doi: 10.1371/journal.pone.0017477 21408173

47. Kim JY, Welsh EA, Oguz U, Fang B, Bai Y, et al. (2013) Dissection of TBK1 signaling via phosphoproteomics in lung cancer cells. Proc Nat Acad Sciences USA 110 : 12414–12419. doi: 10.1073/pnas.1220674110 23836654

48. van Zuylen WJ, Doyon P, Clement JF, Khan KA, D'Ambrosio LM, et al. (2012) Proteomic profiling of the TRAF3 interactome network reveals a new role for the ER-to-Golgi transport compartments in innate immunity. PLoS Pathogens 8: e1002747. doi: 10.1371/journal.ppat.1002747 22792062

49. Kagan JC (2012) Signaling organelles of the innate immune system. Cell 151 : 1168–1178. doi: 10.1016/j.cell.2012.11.011 23217704

50. Suzuki T, Oshiumi H, Miyashita M, Aly HH, Matsumoto M, et al. (2013) Cell type-specific subcellular localization of phospho-TBK1 in response to cytoplasmic viral DNA. PloS One 8: e83639. doi: 10.1371/journal.pone.0083639 24349538

51. West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11 : 389–402. doi: 10.1038/nri2975 21597473

52. Eisenacher K, Krug A (2012) Regulation of RLR-mediated innate immune signaling—it is all about keeping the balance. Europ J Cell Biol 91 : 36–47. doi: 10.1016/j.ejcb.2011.01.011 21481967

53. Goubau D, Deddouche S, Reis e Sousa C (2013) Cytosolic sensing of viruses. Immunity 38 : 855–869. doi: 10.1016/j.immuni.2013.05.007 23706667

54. Zhao W (2013) Negative regulation of TBK1-mediated antiviral immunity. FEBS Lett 587 : 542–548. doi: 10.1016/j.febslet.2013.01.052 23395611

55. Kachaner D, Laplantine E, Genin P, Weil R (2012) Optineurin: a new vision of cell division control. Cell Cycle 11 : 1481–1482. doi: 10.4161/cc.20116 22487679

56. Vitour D, Dabo S, Ahmadi Pour M, Vilasco M, Vidalain PO, et al. (2009) Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J Biol Chem 284 : 21797–21809. doi: 10.1074/jbc.M109.018275 19546225

57. Liu XY, Chen W, Wei B, Shan YF, Wang C (2011) IFN-induced TPR protein IFIT3 potentiates antiviral signaling by bridging MAVS and TBK1. J Immunol 187 : 2559–2568. doi: 10.4049/jimmunol.1100963 21813773

58. Gough DJ, Messina NL, Clarke CJ, Johnstone RW, Levy DE (2012) Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36 : 166–174. doi: 10.1016/j.immuni.2012.01.011 22365663

59. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, et al. (2009) IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458 : 904–908. doi: 10.1038/nature07815 19212321

60. Sato T, Onai N, Yoshihara H, Arai F, Suda T, et al. (2009) Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat Med 15 : 696–700. doi: 10.1038/nm.1973 19483695

61. Takayanagi H, Kim S, Matsuo K, Suzuki H, Suzuki T, et al. (2002) RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature 416 : 744–749. 11961557

62. Hata N, Sato M, Takaoka A, Asagiri M, Tanaka N, et al. (2001) Constitutive IFN-alpha/beta signal for efficient IFN-alpha/beta gene induction by virus. Biochem Biophys Res Comm 285 : 518–525. 11444873

63. Kwon YS, Choe YH, Chin HS (2001) Development of glaucoma in the course of interferon alpha therapy for chronic hepatitis B. Yonsei Med J 42 : 134–136. 11293492

64. Meng Q, Lv J, Ge H, Zhang L, Xue F, et al. (2012) Overexpressed mutant optineurin(E50K) induces retinal ganglion cells apoptosis via the mitochondrial pathway. Mol Biol Rep 39 : 5867–5873. doi: 10.1007/s11033-011-1397-7 22422156

65. Meng Q, Xiao Z, Yuan H, Xue F, Zhu Y, et al. (2012) Transgenic mice with overexpression of mutated human optineurin (E50K) in the retina. Mol Biol Rep 39 : 1119–1124. doi: 10.1007/s11033-011-0840-0 21681420

66. Shen X, Ying H, Qiu Y, Park JS, Shyam R, et al. (2011) Processing of optineurin in neuronal cells. J Biol Chem 286 : 3618–3629. doi: 10.1074/jbc.M110.175810 21059646

67. Cirulli ET, Lasseigne BN, Petrovski S, Sapp PC, Dion PA, et al. (2015) Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science 347 : 1436–1441. doi: 10.1126/science.aaa3650 25700176

68. Freischmidt A, Wieland T, Richter B, Ruf W, Schaeffer V, et al. (2015) Haploinsufficiency of TBK1 causes familial ALS and fronto-temporal dementia. Nat Neuroscience doi: 10.1038/nn.4000

69. Uze G, Di Marco S, Mouchel-Vielh E, Monneron D, Bandu MT, et al. (1994) Domains of interaction between alpha interferon and its receptor components. J Mol Biol 243 : 245–257. 7932753

70. Moretti J, Chastagner P, Liang CC, Cohn MA, Israel A, et al. (2012) The ubiquitin-specific protease 12 (USP12) is a negative regulator of notch signaling acting on notch receptor trafficking toward degradation. J Biol Chem 287 : 29429–29441. doi: 10.1074/jbc.M112.366807 22778262

71. Tarantino N, Tinevez JY, Crowell EF, Boisson B, Henriques R, et al. (2014) TNF and IL-1 exhibit distinct ubiquitin requirements for inducing NEMO-IKK supramolecular structures. Journal Cell Biol 204 : 231–245.