Bid regulates the pathogenesis of neurotropic reovirus

PLoS Pathogens

Volumn 6, Issue 7, 2010, Pages 1-14

  Danthi, Pranav ^a   Pruijssers, Andrea J ^b   Berger, Angela K ^a   Holm, Geoffrey H ^b,c   Zinkel, Sandra S ^b   Dermody, Terence S ^b  

^a INDIANA UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Center for Language and Brain   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN BID; BID PROTEIN, MOUSE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; ENCEPHALITIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PATHOGENESIS; REOVIRUS; REOVIRUS INFECTION; SURVIVAL; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; ANIMAL; DRUG EFFECT; FIBROBLAST; HUMAN; L CELL; PATHOGENICITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY; VIRUS ENCEPHALITIS;

MURINAE; MUS; ORTHOREOVIRUS;

ANIMALS; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; ENCEPHALITIS, VIRAL; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FIBROBLASTS; HUMANS; L CELLS (CELL LINE); MICE; NF-KAPPA B; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; REOVIRIDAE; REOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 77957677378     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000980     Document Type: Article

References (91)

1. Despres P, Frenkiel MP, Ceccaldi PE, Duarte Dos Santos C, Deubel V (1998) Apoptosis in the mouse central nervous system in response to infection with mouse-neurovirulent dengue viruses. J Virol 72: 823-829.
2. Lewis J, Wesselingh SL, Griffin DE, Hardwick JM (1996) Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol 70: 1828-1835.
3. Jackson AC, Rossiter JP (1997) Apoptosis plays an important role in experimental rabies virus infection. J Virol 71: 5603-5607.
4. Danthi P, Kobayashi T, Holm GH, Hansberger MW, Abel TW, et al. (2008) Reovirus apoptosis and virulence are regulated by host cell membrane penetration efficiency. J Virol 82: 161-172.
5. Tyler KL, Squier MKT, Brown AL, Pike B, Willis D, et al. (1996) Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the S1 and M2 genes. J Virol 70: 7984-7991.
6. Tyler KL, Squier MK, Rodgers SE, Schneider SE, Oberhaus SM, et al. (1995) Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein s1. J Virol 69: 6972-6979.
7. Danthi P, Coffey CM, Parker JS, Abel TW, Dermody TS (2008) Independent regulation of reovirus membrane penetration and apoptosis by the mu1 phi domain. PLoS Pathog 4: e1000248.
8. Connolly JL, Rodgers SE, Clarke P, Ballard DW, Kerr LD, et al. (2000) Reovirus-induced apoptosis requires activation of transcription factor NFkappaB. J Virol 74: 2981-2989.
9. Clarke P, Meintzer SM, Widmann C, Johnson GL, Tyler KL (2001) Reovirus infection activates JNK and the JNK-dependent transcription factor c-Jun. J Virol 75: 11275-11283.
10. Clarke P, Meintzer SM, Wang Y, Moffitt LA, Richardson-Burns SM, et al. (2004) JNK regulates the release of proapoptotic mitochondrial factors in reovirus-infected cells. J Virol 78: 13132-13138.
11. O'Donnell SM, Hansberger MW, Connolly JL, Chappell JD, Watson MJ, et al. (2005) Organ-specific roles for transcription factor NF-kB in reovirus-induced apoptosis and disease. J Clin Invest 115: 2341-2350.
12. Beckham JD, Goody RJ, Clarke P, Bonny C, Tyler KL (2007) A novel strategy for the treatment of viral CNS infection utilizing a cell-permeable inhibitor of c-Jun N-terminal kinase. J Virol 81: 6984-6992.
13. Coffey CM, Sheh A, Kim IS, Chandran K, Nibert ML, et al. (2006) Reovirus outer capsid protein m1 induces apoptosis and associates with lipid droplets, endoplasmic reticulum, and mitochondria. J Virol 80: 8422-8438.
14. Danthi P, Hansberger MW, Campbell JA, Forrest JC, Dermody TS (2006) JAM-A-independent, antibody-mediated uptake of reovirus into cells leads to apoptosis. J Virol 80: 1261-1270.
15. Connolly JL, Dermody TS (2002) Virion disassembly is required for apoptosis induced by reovirus. J Virol 76: 1632-1641.
16. Kominsky DJ, Bickel RJ, Tyler KL (2002) Reovirus-induced apoptosis requires both death receptor- and mitochondrial-mediated caspase-dependent pathways of cell death. Cell Death and Diff 9: 926-933.
17. Clarke P, Meintzer SM, Gibson S, Widmann C, Garrington TP, et al. (2000) Reovirus-induced apoptosis is mediated by TRAIL. J Virol 74: 8135-8139.
18. Juo P, Kuo CJ, Yuan J, Blenis J (1998) Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr Biol 8: 1001-1008.
19. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
20. Li P, Nijhawan D, Budhardjo I, Srinivasula SM, Ahmad M, et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
21. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, et al. (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102: 43-53.
22. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42.
23. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, et al. (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410: 549-554.
24. Rodgers SE, Barton ES, Oberhaus SM, Pike B, Gibson CA, et al. (1997) Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bcl-2. J Virol 71: 2540-2546.
25. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ (1990) Bcl-2 is an innner mitochondrial membrane protein that blocks programmed cell death. Nature 348: 334-336.
26. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501.
27. Zha J, Weiler S, Oh KJ, Wei MC, Korsmeyer SJ (2000) Posttranslational Nmyristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290: 1761-1765.
28. Hansberger MW, Campbell JA, Danthi P, Arrate P, Pennington KN, et al. (2007) IkB kinase subunits a and c are required for activation of NF-kB and induction of apoptosis by mammalian reovirus. J Virol 81: 1360-1371.
29. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, et al. (1998) Two CD95 (APO-1/Fas) signaling pathways. Embo J 17: 1675-1687.
30. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, et al. (1999) Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400: 886-891.
31. Mandic A, Viktorsson K, Strandberg L, Heiden T, Hansson J, et al. (2002) Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol Cell Biol 22: 3003-3013.
32. Chen M, He H, Zhan S, Krajewski S, Reed JC, et al. (2001) Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem 276: 30724-30728.
33. Yamada H, Tada-Oikawa S, Uchida A, Kawanishi S (1999) TRAIL causes cleavage of bid by caspase-8 and loss of mitochondrial membrane potential resulting in apoptosis in BJAB cells. Biochem Biophys Res Commun 265: 130-133.
34. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481-490.
35. Gross A, Yin XM, Wang K, Wei MC, Jockel J, et al. (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCLXL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274: 1156-1163.
36. Stoka V, Turk B, Schendel SL, Kim TH, Cirman T, et al. (2001) Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J Biol Chem 276: 3149-3157.
37. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, et al. (2004) Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Diff 11: 550-563.
38. Johansson AC, Steen H, Ollinger K, Roberg K (2003) Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ 10: 1253-1259.
39. Cirman T, Oresic K, Mazovec GD, Turk V, Reed JC, et al. (2004) Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 279: 3578-3587.
40. Debiasi RL, Squier MK, Pike B, Wynes M, Dermody TS, et al. (1999) Reovirusinduced apoptosis is preceded by increased cellular calpain activity and is blocked by calpain inhibitors. J Virol 73: 695-701.
41. Golden JW, Linke J, Schmechel S, Thoemke K, Schiff LA (2002) Addition of exogenous protease facilitates reovirus infection in many restrictive cells. J Virol 76: 7430-7443.
42. Richardson-Burns SM, Kominsky DJ, Tyler KL (2002) Reovirus-induced neuronal apoptosis is mediated by caspase 3 and is associated with the activation of death receptors. J Neurovirol 8: 365-380.
43. Clarke P, Beckham JD, Leser JS, Hoyt CC, Tyler KL (2009) Fas-mediated apoptotic signaling in the mouse brain following reovirus infection. J Virol 83: 6161-6170.
44. Yujiri T, Ware M, Widmann C, Oyer R, Russell D, et al. (2000) MEK kinase 1 gene disruption alters cell migration and c-Jun NH2-terminal kinase regulation but does not cause a measurable defect in NF-kappa B activation. Proc Natl Acad Sci U S A 97: 7272-7277.
45. Diehl GE, Yue HH, Hsieh K, Kuang AA, Ho M, et al. (2004) TRAIL-R as a negative regulator of innate immune cell responses. Immunity 21: 877-889.
46. Finnberg N, Gruber JJ, Fei P, Rudolph D, Bric A, et al. (2005) DR5 knockout mice are compromised in radiation-induced apoptosis. Mol Cell Biol 25: 2000-2013.
47. Finnberg N, Klein-Szanto AJ, El-Deiry WS (2008) TRAIL-R deficiency in mice promotes susceptibility to chronic inflammation and tumorigenesis. J Clin Invest 118: 111-123.
48. Richardson-Burns SM, Tyler KL (2004) Regional differences in viral growth and central nervous system injury correlate with apoptosis. J Virol 78: 5466-5475.
49. Richardson-Burns SM, Tyler KL (2005) Minocycline delays disease onset and mortality in reovirus encephalitis. Exp Neurol 192: 331-339.
50. Barton ES, Youree BE, Ebert DH, Forrest JC, Connolly JL, et al. (2003) Utilization of sialic acid as a coreceptor is required for reovirus-induced biliary disease. J Clin Invest 111: 1823-1833.
51. Antar AA, Konopka JL, Campbell JA, Henry RA, Perdigoto AL, et al. (2009) Junctional adhesion molecule-A is required for hematogenous dissemination of reovirus. Cell Host Microbe 5: 59-71.
52. Gadaleta P, Perfetti X, Mersich S, Coulombie F (2005) Early activation of the mitochondrial apoptotic pathway in Vesicular Stomatitis virus-infected cells. Virus Res 109: 65-69.
53. Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P (2005) Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1: e4.
54. Jan JT, Chen BH, Ma SH, Liu CI, Tsai HP, et al. (2000) Potential dengue virustriggered apoptotic pathway in human neuroblastoma cells: arachidonic acid, superoxide anion, and NF-kappaB are sequentially involved. J Virol 74: 8680-8691.
55. Perfettini JL, Castedo M, Roumier T, Andreau K, Nardacci R, et al. (2005) Mechanisms of apoptosis induction by the HIV-1 envelope. Cell Death Differ 12 Suppl 1: 916-923.
56. Liu M, Vakharia VN (2006) Nonstructural protein of infectious bursal disease virus inhibits apoptosis at the early stage of virus infection. J Virol 80: 3369-3377.
57. Lin KI, Lee SH, Narayanan R, Baraban J, Hardwick J, et al. (1995) Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappa B. J Cell Biol 131: 1149-1161.
58. Tyler KL, Squier MK, Brown AL, Pike B, Willis D, et al. (1996) Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the S1 and M2 genes. J Virol 70: 7984-7991.
59. DeBiasi RL, Clarke P, Meintzer SM, Jotte RM, Kleinschmidt-Demasters BK, et al. (2003) Reovirus-induced alteration in expression of apoptosis and DNA repair genes with potential roles in viral pathogenesis. J Virol 77: 8934-8947.
60. Sherry B, Torres J, Blum MA (1998) Reovirus induction of and sensitivity to beta interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J Virol 72: 1314-1323.
61. O'Donnell SM, Holm GH, Pierce JM, Tian B, Watson MJ, et al. (2006) Identification of an NF-kB-dependent gene network in cells infected by mammalian reovirus. J Virol 80: 1077-1086.
62. Smith JA, Schmechel SC, Raghavan A, Abelson M, Reilly C, et al. (2006) Reovirus induces and benefits from an integrated cellular stress response. J Virol 80: 2019-2033.
63. Rivera-Walsh I, Waterfield M, Xiao G, Fong A, Sun SC (2001) NF-kappaB signaling pathway governs TRAIL gene expression and human T-cell leukemia virus-I Tax-induced T-cell death. J Biol Chem 276: 40385-40388.
64. Harwood FG, Kasibhatla S, Petak I, Vernes R, Green DR, et al. (2000) Regulation of FasL by NF-kappaB and AP-1 in Fas-dependent thymineless death of human colon carcinoma cells. J Biol Chem 275: 10023-10029.
65. Kasibhatla S, Brunner T, Genestier L, Echeverri F, Mahboubi A, et al. (1998) DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol Cell 1: 543-551.
66. Kasibhatla S, Genestier L, Green DR (1999) Regulation of fas-ligand expression during activation-induced cell death in T lymphocytes via nuclear factor kappaB. J Biol Chem 274: 987-992.
67. Shou Y, Li N, Li L, Borowitz JL, Isom GE (2002) NF-kappaB-mediated upregulation of Bcl-X(S) and Bax contributes to cytochrome c release in cyanideinduced apoptosis. J Neurochem 81: 842-852.
68. Belov GA, Romanova LI, Tolskaya EA, Kolesnikova MS, Lazebnik YA, et al. (2003) The major apoptotic pathway activated and suppressed by poliovirus. J Virol 77: 45-56.
69. Chen CJ, Makino S (2002) Murine coronavirus-induced apoptosis in 17Cl-1 cells involves a mitochondria-mediated pathway and its downstream caspase-8 activation and bid cleavage. Virology 302: 321-332.
70. Chiou HL, Hsieh YS, Hsieh MR, Chen TY (2006) HCV E2 may induce apoptosis of Huh-7 cells via a mitochondrial-related caspase pathway. Biochem Biophys Res Commun 345: 453-458.
71. Lee SM, Kleiboeker SB (2007) Porcine reproductive and respiratory syndrome virus induces apoptosis through a mitochondria-mediated pathway. Virology 365: 419-434.
72. Lin CH, Shih WL, Lin FL, Hsieh YC, Kuo YR, et al. (2009) Bovine ephemeral fever virus-induced apoptosis requires virus gene expression and activation of Fas and mitochondrial signaling pathway. Apoptosis 14: 864-877.
73. Liu Y, Pu Y, Zhang X (2006) Role of the mitochondrial signaling pathway in murine coronavirus-induced oligodendrocyte apoptosis. J Virol 80: 395-403.
74. Padhan K, Minakshi R, Towheed MA, Jameel S (2008) Severe acute respiratory syndrome coronavirus 3a protein activates the mitochondrial death pathway through p38 MAP kinase activation. J Gen Virol 89: 1960-1969.
75. St-Louis MC, Archambault D (2007) The equine arteritis virus induces apoptosis via caspase-8 and mitochondria-dependent caspase-9 activation. Virology 367: 147-155.
76. Tun C, Guo W, Nguyen H, Yun B, Libby RT, et al. (2007) Activation of the extrinsic caspase pathway in cultured cortical neurons requires p53-mediated down-regulation of the X-linked inhibitor of apoptosis protein to induce apoptosis. J Neurochem 102: 1206-1219.
77. Ubol S, Kasisith J, Pitidhammabhorn D, Tepsumethanol V (2005) Screening of pro-apoptotic genes upregulated in an experimental street rabies virus-infected neonatal mouse brain. Microbiol Immunol 49: 423-431.
78. Urban C, Rheme C, Maerz S, Berg B, Pick R, et al. (2008) Apoptosis induced by Semliki Forest virus is RNA replication dependent and mediated via Bak. Cell Death Differ 15: 1396-1407.
79. Pearce AF, Lyles DS (2009) Vesicular stomatitis virus induces apoptosis primarily through Bak rather than Bax by inactivating Mcl-1 and Bcl- XL. J Virol.
80. Fischer SF, Belz GT, Strasser A (2008) BH3-only protein Puma contributes to death of antigen-specific T cells during shutdown of an immune response to acute viral infection. Proc Natl Acad Sci U S A 105: 3035-3040.
81. Becattini B, Sareth S, Zhai D, Crowell KJ, Leone M, et al. (2004) Targeting apoptosis via chemical design: inhibition of bid-induced cell death by small organic molecules. Chem Biol 11: 1107-1117.
82. Becattini B, Culmsee C, Leone M, Zhai D, Zhang X, et al. (2006) Structureactivity relationships by interligand NOE-based design and synthesis of antiapoptotic compounds targeting Bid. Proc Natl Acad Sci U S A 103: 12602-12606.
83. Landshamer S, Hoehn M, Barth N, Duvezin-Caubet S, Schwake G, et al. (2008) Bid-induced release of AIF from mitochondria causes immediate neuronal cell death. Cell Death Differ 15: 1553-1563.
84. Barton ES, Connolly JL, Forrest JC, Chappell JD, Dermody TS (2001) Utilization of sialic acid as a coreceptor enhances reovirus attachment by multistep adhesion strengthening. J Biol Chem 276: 2200-2211.
85. Furlong DB, Nibert ML, Fields BN (1988) Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol 62: 246-256.
86. Smith RE, Zweerink HJ, Joklik WK (1969) Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39: 791-810.
87. Wetzel JD, Chappell JD, Fogo AB, Dermody TS (1997) Efficiency of viral entry determines the capacity of murine erythroleukemia cells to support persistent infections by mammalian reoviruses. J Virol 71: 299-306.
88. Carter RS, Geyer BC, Xie M, Acevedo-Suarez CA, Ballard DW (2001) Persistent activation of NF-kB by the tax transforming protein involves chronic phosphorylation of IkB kinase subunits IKKb and IKKc. J Biol Chem 276: 24445-24448.
89. Virgin HW, IV, Bassel-Duby R, Fields BN, Tyler KL (1988) Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol 62: 4594-4604.
90. Tyler KL, Bronson RT, Byers KB, Fields BN (1985) Molecular basis of viral neurotropism: experimental reovirus infection. Neurology 35: 88-92.
91. Rubin DH, Fields BN (1980) Molecular basis of reovirus virulence: role of the M2 gene. J Exp Med 152: 853-868.