Entrapment of viral capsids in nuclear PML cages is an intrinsic antiviral host defense against Varicella-zoster virus

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Reichelt, Mike ^a   Wang, Li ^a   Sommer, Marvin ^a   Perrino, John ^a   Nour, Adel M ^a   Sen, Nandini ^a   Baiker, Armin ^b   Zerboni, Leigh ^a   Arvin, Ann M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; HUNTINGTIN; PROMYELOCYTIC LEUKEMIA PROTEIN; NUCLEAR PROTEIN; PML PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; HERPES ZOSTER; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IN VIVO STUDY; NERVE CELL; NONHUMAN; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SATELLITE CELL; SKIN CELL; SPINAL GANGLION; VARICELLA ZOSTER VIRUS; VIRUS CAPSID; VIRUS NUCLEOCAPSID; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL NUCLEUS; CELL PROTECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PROTEIN BINDING; PROTEIN MULTIMERIZATION; VIROLOGY; VIRUS INCLUSION; XENOGRAFT;

DNA VIRUSES; HERPESVIRIDAE; HUMAN HERPESVIRUS 3; MIRIDAE;

ANIMALS; CAPSID; CELL NUCLEUS; CELLS, CULTURED; CYTOPROTECTION; EMBRYO, MAMMALIAN; HERPESVIRUS 3, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; INCLUSION BODIES, VIRAL; INTRANUCLEAR INCLUSION BODIES; MICE; MICE, SCID; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; TUMOR SUPPRESSOR PROTEINS;

EID: 79952219169     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001266     Document Type: Article

References (93)

1. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, et al. (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 147: 221-234.
2. Zhong S, Muller S, Ronchetti S, Freemont PS, Dejean A, et al. (2000) Role of SUMO-1-modified PML in nuclear body formation. Blood 95: 2748-2752.
3. Lallemand-Breitenbach V, Zhu J, Puvion F, Koken M, Honore N, et al. (2001) Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J Exp Med 193: 1361-1371.
4. Eskiw CH, Dellaire G, Mymryk JS, Bazett-Jones DP, (2003) Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly. J Cell Sci 116: 4455-4466.
5. Muratani M, Gerlich D, Janicki SM, Gebhard M, Eils R, et al. (2002) Metabolic-energy-dependent movement of PML bodies within the mammalian cell nucleus. Nat Cell Biol 4: 106-110.
6. Brand P, Lenser T, Hemmerich P, (2010) Assembly dynamics of PML nuclear bodies in living cells. PMC Biophys 3: 3.
7. Zhong S, Salomoni P, Pandolfi PP, (2000) The transcriptional role of PML and the nuclear body. Nat Cell Biol 2: E85-90.
8. Dellaire G, Bazett-Jones DP, (2004) PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26: 963-977.
9. Takahashi Y, Lallemand-Breitenbach V, Zhu J, de The H, (2004) PML nuclear bodies and apoptosis. Oncogene 23: 2819-2824.
10. Bernardi R, Pandolfi PP, (2003) Role of PML and the PML-nuclear body in the control of programmed cell death. Oncogene 22: 9048-9057.
11. Lallemand-Breitenbach V, de The H, (2010) PML nuclear bodies. 2 (5) Cold Spring Harb Perspect Biol.
12. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, et al. (2010) PML Regulates Apoptosis at Endoplasmic Reticulum by Modulating Calcium Release. Science 330: 1183-1184.
13. Fagioli M, Alcalay M, Pandolfi PP, Venturini L, Mencarelli A, et al. (1992) Alternative splicing of PML transcripts predicts coexpression of several carboxy-terminally different protein isoforms. Oncogene 7: 1083-1091.
14. Jensen K, Shiels C, Freemont PS, (2001) PML protein isoforms and the RBCC/TRIM motif. Oncogene 20: 7223-7233.
15. Kastner P, Perez A, Lutz Y, Rochette-Egly C, Gaub MP, et al. (1992) Structure, localization and transcriptional properties of two classes of retinoic acid receptor alpha fusion proteins in acute promyelocytic leukemia (APL): structural similarities with a new family of oncoproteins. Embo J 11: 629-642.
16. Beech SJ, Lethbridge KJ, Killick N, McGlincy N, Leppard KN, (2005) Isoforms of the promyelocytic leukemia protein differ in their effects on ND10 organization. Exp Cell Res 307: 109-117.
17. Condemine W, Takahashi Y, Zhu J, Puvion-Dutilleul F, Guegan S, et al. (2006) Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res 66: 6192-6198.
18. Weidtkamp-Peters S, Lenser T, Negorev D, Gerstner N, Hofmann TG, et al. (2008) Dynamics of component exchange at PML nuclear bodies. J Cell Sci 121: 2731-2743.
19. Everett RD, Chelbi-Alix MK, (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89: 819-830.
20. Tavalai N, Stamminger T, (2008) New insights into the role of the subnuclear structure ND10 for viral infection. Biochim Biophys Acta 1783: 2207-2221.
21. Pellett PE, Roizman B, (2007) The Family: Herpesviridae, A Brief Introduction. In: Knipe DM, Howley PM, editors. Fields Virology Philadelphia Lippincott Williams and Wilkins, a Wolters Kluwer Business pp. 2479-2500 5 ed.
22. Mettenleiter TC, Klupp BG, Granzow H, (2009) Herpesvirus assembly: an update. Virus Res 143: 222-234.
23. Everett RD, Rechter S, Papior P, Tavalai N, Stamminger T, et al. (2006) PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J Virol 80: 7995-8005.
24. Tavalai N, Papior P, Rechter S, Leis M, Stamminger T, (2006) Evidence for a role of the cellular ND10 protein PML in mediating intrinsic immunity against human cytomegalovirus infections. J Virol 80: 8006-8018.
25. Maul GG, Guldner HH, Spivack JG, (1993) Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J Gen Virol 74: 2679-2690.
26. Everett RD, Maul GG, (1994) HSV-1 IE protein Vmw110 causes redistribution of PML. Embo J 13: 5062-5069.
27. Chelbi-Alix MK, de The H, (1999) Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18: 935-941.
28. Boutell C, Sadis S, Everett RD, (2002) Herpes simplex virus type 1 immediate-early protein ICP0 and is isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol 76: 841-850.
29. Chee AV, Lopez P, Pandolfi PP, Roizman B, (2003) Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J Virol 77: 7101-7105.
30. Cohen JI, Straus SE, Arvin AM, (2007) Varicella-Zoster Virus. In: Knipe DM, Howley PM, editors. Fields Virology Philadelphia Lippincott Williams and Wilkins, a Wolters Kluwer Business pp. 2773-2818 5 ed.
31. Kyratsous CA, Silverstein SJ, (2009) Components of nuclear domain 10 bodies regulate varicella-zoster virus replication. J Virol 83: 4262-4274.
32. Reichelt M, Brady J, Arvin AM, (2009) The replication cycle of varicella-zoster virus: analysis of the kinetics of viral protein expression, genome synthesis, and virion assembly at the single-cell level. J Virol 83: 3904-3918.
33. Mueller NH, Gilden DH, Cohrs RJ, Mahalingam R, Nagel MA, (2008) Varicella zoster virus infection: clinical features, molecular pathogenesis of disease, and latency. Neurol Clin 26: 675-697.
34. Moffat JF, Stein MD, Kaneshima H, Arvin AM, (1995) Tropism of varicella-zoster virus for human CD4+ and CD8+ T lymphocytes and epidermal cells in SCID-hu mice. J Virol 69: 5236-5242.
35. Moffat JF, Zerboni L, Sommer MH, Heineman TC, Cohen JI, et al. (1998) The ORF47 and ORF66 putative protein kinases of varicella-zoster virus determine tropism for human T cells and skin in the SCID-hu mouse. Proc Natl Acad Sci U S A 95: 11969-11974.
36. Zerboni L, Ku CC, Jones CD, Zehnder JL, Arvin AM, (2005) Varicella-zoster virus infection of human dorsal root ganglia in vivo. Proc Natl Acad Sci U S A 102: 6490-6495.
37. Arvin AM, Moffat J, Sommer M, Oliver S, Che X, et al. (2010) Varicella-Zoster Virus T Cell Tropism and the Pathogenesis of Skin Infection. Curr Top Microbiol Immunol 342: 189-209.
38. Zerboni L, Reichelt M, Arvin A, (2010) Varicella-Zoster Virus Neurotropism in SCID Mouse-Human Dorsal Root Ganglia Xenografts. Curr Top Microbiol Immunol 342: 255-276.
39. Ku CC, Zerboni L, Ito H, Graham BS, Wallace M, et al. (2004) Varicella-zoster virus transfer to skin by T Cells and modulation of viral replication by epidermal cell interferon-alpha. J Exp Med 200: 917-925.
40. Skinner PJ, Koshy BT, Cummings CJ, Klement IA, Helin K, et al. (1997) Ataxin-1 with an expanded glutamine tract alters nuclear matrix-associated structures. Nature 389: 971-974.
41. Yamada M, Sato T, Shimohata T, Hayashi S, Igarashi S, et al. (2001) Interaction between neuronal intranuclear inclusions and promyelocytic leukemia protein nuclear and coiled bodies in CAG repeat diseases. Am J Pathol 159: 1785-1795.
42. Takahashi J, Fujigasaki H, Zander C, El Hachimi KH, Stevanin G, et al. (2002) Two populations of neuronal intranuclear inclusions in SCA7 differ in size and promyelocytic leukaemia protein content. Brain 125: 1534-1543.
43. Takahashi J, Fujigasaki H, Iwabuchi K, Bruni AC, Uchihara T, et al. (2003) PML nuclear bodies and neuronal intranuclear inclusion in polyglutamine diseases. Neurobiol Dis 13: 230-237.
44. Janer A, Martin E, Muriel MP, Latouche M, Fujigasaki H, et al. (2006) PML clastosomes prevent nuclear accumulation of mutant ataxin-7 and other polyglutamine proteins. J Cell Biol 174: 65-76.
45. Woulfe J, (2008) Nuclear bodies in neurodegenerative disease. Biochim Biophys Acta 1783: 2195-2206.
46. Williams AJ, Paulson HL, (2008) Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci 31: 521-528.
47. Yasuda S, Inoue K, Hirabayashi M, Higashiyama H, Yamamoto Y, et al. (1999) Triggering of neuronal cell death by accumulation of activated SEK1 on nuclear polyglutamine aggregations in PML bodies. Genes Cells 4: 743-756.
48. Villagra NT, Navascues J, Casafont I, Val-Bernal JF, Lafarga M, et al. (2006) The PML-nuclear inclusion of human supraoptic neurons: a new compartment with SUMO-1- and ubiquitin-proteasome-associated domains. Neurobiol Dis 21: 181-193.
49. Lafarga M, Berciano MT, Pena E, Mayo I, Castano JG, et al. (2002) Clastosome: a subtype of nuclear body enriched in 19S and 20S proteasomes, ubiquitin, and protein substrates of proteasome. Mol Biol Cell 13: 2771-2782.
50. Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S, (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431: 805-810.
51. Qin Q, Inatome R, Hotta A, Kojima M, Yamamura H, et al. (2006) A novel GTPase, CRAG, mediates promyelocytic leukemia protein-associated nuclear body formation and degradation of expanded polyglutamine protein. J Cell Biol 172: 497-504.
52. Torashima T, Koyama C, Iizuka A, Mitsumura K, Takayama K, et al. (2008) Lentivector-mediated rescue from cerebellar ataxia in a mouse model of spinocerebellar ataxia. EMBO Rep 9: 393-399.
53. Stuurman N, de Graaf A, Floore A, Josso A, Humbel B, et al. (1992) A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies. J Cell Sci 101 (Pt 4): 773-784.
54. Chaudhuri V, Sommer M, Rajamani J, Zerboni L, Arvin AM, (2008) Functions of Varicella-zoster virus ORF23 capsid protein in viral replication and the pathogenesis of skin infection. J Virol 82: 10231-10246.
55. Everett RD, Sourvinos G, Leiper C, Clements JB, Orr A, (2004) Formation of nuclear foci of the herpes simplex virus type 1 regulatory protein ICP4 at early times of infection: localization, dynamics, recruitment of ICP27, and evidence for the de novo induction of ND10-like complexes. J Virol 78: 1903-1917.
56. Wileman T, (2007) Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu Rev Microbiol 61: 149-167.
57. Day PM, Roden RB, Lowy DR, Schiller JT, (1998) The papillomavirus minor capsid protein, L2, induces localization of the major capsid protein, L1, and the viral transcription/replication protein, E2, to PML oncogenic domains. J Virol 72: 142-150.
58. Florin L, Schafer F, Sotlar K, Streeck RE, Sapp M, (2002) Reorganization of nuclear domain 10 induced by papillomavirus capsid protein l2. Virology 295: 97-107.
59. Shishido-Hara Y, Ichinose S, Higuchi K, Hara Y, Yasui K, (2004) Major and minor capsid proteins of human polyomavirus JC cooperatively accumulate to nuclear domain 10 for assembly into virions. J Virol 78: 9890-9903.
60. Puvion-Dutilleul F, Venturini L, Guillemin MC, de The H, Puvion E, (1995) Sequestration of PML and Sp100 proteins in an intranuclear viral structure during herpes simplex virus type 1 infection. Exp Cell Res 221: 448-461.
61. Tokuyasu KT, (1973) A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57: 551-565.
62. Griffiths G, Simons K, Warren G, Tokuyasu KT, (1983) Immunoelectron microscopy using thin, frozen sections: application to studies of the intracellular transport of Semliki Forest virus spike glycoproteins. Methods Enzymol 96: 466-485.
63. Webster P, Schwarz H, Griffiths G, (2008) Preparation of cells and tissues for immuno EM. Methods Cell Biol 88: 45-58.
64. Zhou ZH, He J, Jakana J, Tatman JD, Rixon FJ, et al. (1995) Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat Struct Biol 2: 1026-1030.
65. Zhou ZH, Dougherty M, Jakana J, He J, Rixon FJ, et al. (2000) Seeing the herpesvirus capsid at 8.5 A. Science 288: 877-880.
66. McDonald KentL, Morphew Mary, Verkade Paul, Mueller-Reichert Thomas, (2007) Recent Advances in High-Pressure Freezing: Equipment and Specimen-Loading Methods. In: Kuo J, editors. Methods In Molecular Biology: Electron Microscopy, Methods and Protocols Totowa, New Jersey Humana Press pp. 143-173 2 ed.
67. Rabouille C, (1999) Quantitative aspects of immunogold labeling in embedded and nonembedded sections. Methods Mol Biol 117: 125-144.
68. Gilden DH, Rozenman Y, Murray R, Devlin M, Vafai A, (1987) Detection of varicella-zoster virus nucleic acid in neurons of normal human thoracic ganglia. Ann Neurol 22: 377-380.
69. Levin MJ, Cai GY, Manchak MD, Pizer LI, (2003) Varicella-zoster virus DNA in cells isolated from human trigeminal ganglia. J Virol 77: 6979-6987.
70. Wang K, Lau TY, Morales M, Mont EK, Straus SE, (2005) Laser-capture microdissection: refining estimates of the quantity and distribution of latent herpes simplex virus 1 and varicella-zoster virus DNA in human trigeminal Ganglia at the single-cell level. J Virol 79: 14079-14087.
71. Moriuchi H, Moriuchi M, Smith HA, Cohen JI, (1994) Varicella-zoster virus open reading frame 4 protein is functionally distinct from and does not complement its herpes simplex virus type 1 homolog, ICP27. J Virol 68: 1987-1992.
72. Defechereux P, Debrus S, Baudoux L, Rentier B, Piette J, (1997) Varicella-zoster virus open reading frame 4 encodes an immediate-early protein with posttranscriptional regulatory properties. J Virol 71: 7073-7079.
73. Homa FL, Brown JC, (1997) Capsid assembly and DNA packaging in herpes simplex virus. Rev Med Virol 7: 107-122.
74. Chen JJ, Zhu Z, Gershon AA, Gershon MD, (2004) Mannose 6-phosphate receptor dependence of varicella zoster virus infection in vitro and in the epidermis during varicella and zoster. Cell 119: 915-926.
75. Iwata A, Christianson JC, Bucci M, Ellerby LM, Nukina N, et al. (2005) Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc Natl Acad Sci U S A 102: 13135-13140.
76. Burkham J, Coen DM, Hwang CB, Weller SK, (2001) Interactions of herpes simplex virus type 1 with ND10 and recruitment of PML to replication compartments. J Virol 75: 2353-2367.
77. Everett RD, Murray J, (2005) ND10 components relocate to sites associated with herpes simplex virus type 1 nucleoprotein complexes during virus infection. J Virol 79: 5078-5089.
78. Delhaye S, Paul S, Blakqori G, Minet M, Weber F, et al. (2006) Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci U S A 103: 7835-7840.
79. Forest T, Barnard S, Baines JD, (2005) Active intranuclear movement of herpesvirus capsids. Nat Cell Biol 7: 429-431.
80. Feierbach B, Piccinotti S, Bisher M, Denk W, Enquist LW, (2006) Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog 2: e85.
81. Lopez P, Jacob RJ, Roizman B, (2002) Overexpression of promyelocytic leukemia protein precludes the dispersal of ND10 structures and has no effect on accumulation of infectious herpes simplex virus 1 or its proteins. J Virol 76: 9355-9367.
82. Day PM, Baker CC, Lowy DR, Schiller JT, (2004) Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc Natl Acad Sci U S A 101: 14252-14257.
83. Shishido-Hara Y, Higuchi K, Ohara S, Duyckaerts C, Hauw JJ, et al. (2008) Promyelocytic leukemia nuclear bodies provide a scaffold for human polyomavirus JC replication and are disrupted after development of viral inclusions in progressive multifocal leukoencephalopathy. J Neuropathol Exp Neurol 67: 299-308.
84. Haller O, Stertz S, Kochs G, (2007) The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect 9: 1636-1643.
85. Kochs G, Janzen C, Hohenberg H, Haller O, (2002) Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes. Proc Natl Acad Sci U S A 99: 3153-3158.
86. Reichelt M, Stertz S, Krijnse-Locker J, Haller O, Kochs G, (2004) Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes. Traffic 5: 772-784.
87. Schunemann S, Mainka C, Wolff MH, (1998) Subclinical reactivation of varicella-zoster virus in immunocompromised and immunocompetent individuals. Intervirology 41: 98-102.
88. Reichelt M, Zerboni L, Arvin AM, (2008) Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia. J Virol 82: 3971-3983.
89. Au WY, Kwong YL, (2005) Frequent varicella zoster reactivation associated with therapeutic use of arsenic trioxide: portents of an old scourge. J Am Acad Dermatol 53: 890-892.
90. Nouri K, Ricotti CA Jr, Bouzari N, Chen H, Ahn E, et al. (2006) The incidence of recurrent herpes simplex and herpes zoster infection during treatment with arsenic trioxide. J Drugs Dermatol 5: 182-185.
91. Jeanne M, Lallemand-Breitenbach V, Ferhi O, Koken M, Le Bras M, et al. (2010) PML/RARA oxidation and arsenic binding initiate the antileukemia response of As2O3. Cancer Cell 18: 88-98.
92. Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, et al. (2010) Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science 328: 240-243.
93. Vizoso Pinto MG, Villegas JM, Peter J, Haase R, Haas J, et al. (2009) LuMPIS-a modified luminescence-based mammalian interactome mapping pull-down assay for the investigation of protein-protein interactions encoded by GC-low ORFs. Proteomics 9: 5303-5308.