Reovirus-induced neuronal apoptosis is mediated by caspase 3 and is associated with the activation of death receptors

References

• Allsopp TE, Fazakerley JK (2000). Altruistic cell suicide and the specialized case of the virus-infected nervous system. Trends Neurosci 23: 284–290.
   PubMedGoogle Scholar
• Ashkenazi A, Dixit VM (1998). Death receptors: Signaling and modulation. Science 281: 1305–1308.
   PubMed Web of Science ®Google Scholar
• Bitzer M, Prinz F, Bauer M, Spiegel M, Neubert WJ, Gregor M, Schulze-Osthoff K, Lauer U (1999). Sendai virus in-fection induces apoptosis through activation of caspase-8 (FLICE) and caspase-3 (CPP32). I Virol 73: 702–708.
   Web of Science ®Google Scholar
• Budd SL, Lipton SA (1999). Signaling events in NMDA receptor-induced apoptosis in cerebrocortical cultures. Ann N Y Acad Sci 893: 261–264.
   Google Scholar
• Chien CT, Hsu SM, Chen CF, Lee PH, Lai MK (2000). Pro-longed ischemia potentiates apoptosis formation during reperfusion by increase of caspase 3 activity and free radical generation. Transplant Proc 32: 2065–2066.
   Google Scholar
• Clarke P, Meintzer SM, Gibson S, Widmann C, Garrington TP, Johnson GL, Tyler KL (2000). Reovirus-induced apoptosis is mediated by TRAIL. I Virol 74: 8135–8139.
   PubMed Web of Science ®Google Scholar
• Clarke P, Meintzer SM, Spalding AC, Johnson GL, Tyler KL (2001). Caspase 8-dependent sensitization of cancer cells to TRAIL-induced apoptosis following reovirus-infection. Oncogene 20: 6910–6919.
   Google Scholar
• DeBiasi RL, Edelstein CL, Sherry B, Tyler KL (2001). Cal-pain inhibition protects against virus-induced apoptotic myocardial injury. I Virol 75: 351–361.
   PubMed Web of Science ®Google Scholar
• DeBiasi RL, Squier MK, Pike B, Wynes M, Dermody TS, Cohen JJ, Tyler KL (1999). Reovirus-induced apopto-sis is preceded by increased cellular calpain activity and is blocked by calpain inhibitors. J Virol 73: 695–701.
   PubMed Web of Science ®Google Scholar
• D'Mello SR, Kuan CY, Flavell RA, Rakic P (2000). Caspase-3 is required for apoptosis-associated DNA fragmentation but not for cell death in neurons deprived of potassium. J Neurosci Res 59: 24–31.
   PubMed Web of Science ®Google Scholar
• Despres P, Flamand M, Ceccaldi PE, Deubel V (1996). Hu-man isolates of dengue type 1 virus induce apoptosis in mouse neuroblastoma cells. I Virol 70: 4090–4096.
   Google Scholar
• Dorr J, Bechmann I, Waiczies S, Aktas O, Walczak H, Krammer PH, Nitsch R, Zipp F (2002). Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. I Neurosci 22: RC209.
   Google Scholar
• Earnshaw WC, Martins LM, Kaufmann SH (1999). Mam-malian caspases: Structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383–424.
   PubMed Web of Science ®Google Scholar
• Gavrieli Y, Sherman Y, Ben Sasson SA (1992). Identifica-tion of programmed cell death in situ via specific label-ing of nuclear DNA fragmentation. I Cell Biol 119: 493–501.
   Google Scholar
• Girard S, Couderc T, Destombes J, Thiesson D, Delpeyroux F, Blondel B (1999). Poliovirus induces apoptosis in the mouse central nervous system. I Virol 73: 6066–6072.
   PubMedGoogle Scholar
• Gong J, Traganos F, Darzynkiewicz Z (1994). A selective procedure for DNA extraction from apoptotic cells ap-plicable for gel electrophoresis and flow cytometry. Anal Biochem 218: 314–319.
   PubMed Web of Science ®Google Scholar
• Gray F, Adle-Biassette H, Brion F, Ereau T, Le MI, Levy V, Corcket G (2000). Neuronal apoptosis in human im-munodeficiency virus infection. J Neurovirol 6(Suppl 1): S38–S43.
   Google Scholar
• Gupta S (2000). Molecular steps of cell suicide: An insight into immune senescence. I Clin Immunol 20: 229–239.
   Web of Science ®Google Scholar
• Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, Shimizu-Sasamata M, Yuan J, Moskowitz MA (1997). Inhibition of interleukin 1beta converting en-zyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Nail Acad Sci USA 94: 2007–2012.
   Google Scholar
• Hengartner MO (2000). The biochemistry of apoptosis. Nature 407: 770–776.
   PubMed Web of Science ®Google Scholar
• Honig LS, Rosenberg RN (2000). Apoptosis and neurologic disease. Am J Med 108: 317–330.
   PubMed Web of Science ®Google Scholar
• Jackson AC, Rossiter JP (1997a). Apoptosis plays an impor-tant role in experimental rabies virus infection. J Virol 71: 5603–5607.
   PubMed Web of Science ®Google Scholar
• Jackson AC, Rossiter JP (1997b). Apoptotic cell death is an important cause of neuronal injury in experimental Venezuelan equine encephalitis virus infection of mice. Acta Neuropathol (Berl) 93: 349–353.
   PubMed Web of Science ®Google Scholar
• Jackson AC, SenGupta SK, Smith JF (1991). Pathogenesis of Venezuelan equine encephalitis virus infection in mice and hamsters. Vet Pathol 28: 410–418.
   PubMed Web of Science ®Google Scholar
• Jan JT, Chatterjee S, Griffin DE (2000). Sindbis virus entry into cells triggers apoptosis by activating sphingomyeli-nase, leading to the release of ceramide. I Virol 74: 6425–6432.
   Web of Science ®Google Scholar
• Jan JT, Griffin DE (1999). Induction of apoptosis by Sind-bis virus occurs at cell entry and does not require virus replication. I Virol 73: 10296–10302.
   PubMed Web of Science ®Google Scholar
• Jelachich ML, Lipton HL (2001). Theiler's murine en-cephalomyelitis virus induces apoptosis in gamma interferon-activated M1 differentiated myelomonocytic cells through a mechanism involving tumor necrosis fac-tor alpha (TNF-alpha) and TNF-alpha-related apoptosis-inducing ligand. I Virol 75: 5930–5938.
   PubMed Web of Science ®Google Scholar
• Jiang D, Jha N, Boonplueang R, Andersen JK (2001). Cas-pase 3 inhibition attenuates hydrogen peroxide-induced DNA fragmentation but not cell death in neuronal PC12 cells. J Neurochem 76: 1745–1755.
   PubMed Web of Science ®Google Scholar
• Kaul M, Garden GA, Lipton SA (2001). Pathways to neu-ronal injury and apoptosis in HIV-associated dementia. Nature 410: 988–994.
   PubMed Web of Science ®Google Scholar
• Kominsky DJ, Bickel RJ, Tyler KL (2002). Reovirus-induced apoptosis requires both death receptor and mitochondria-mediated caspase-dependent pathways of cell death. Cell Death Differ 9: 926–933.
   PubMed Web of Science ®Google Scholar
• Kondratyev A, Gale K (2000). Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res Mol Brain Res 75: 216–224.
   PubMedGoogle Scholar
• Lewis J, Wesselingh SL, Griffin DE, Hardwick JM (1996). Alphavirus-induced apoptosis in mouse brains corre-lates with neurovirulence. I Virol 70: 1828–1835.
   PubMed Web of Science ®Google Scholar
• Li P, Nijhawan D, Budihardj o I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex ini-tiates an apoptotic protease cascade. Cell 91: 479–489.
   Google Scholar
• Lopez-Guerrer o JA, Alonso M, Martin-Belmonte F, Carrasco L (2000). Poliovirus induces apoptosis in the human U937 promonocytic cell line. Virology 272: 250–256.
   Google Scholar
• Ma J, Endres M, Moskowitz MA (1998). Synergistic ef-fects of caspase inhibitors and MK-801 in brain injury after transient focal cerebral ischaemia in mice. Br I Pharmacol 124: 756–762.
   PubMed Web of Science ®Google Scholar
• Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR (1995). Early re-distribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bc1-2 and Abl. J Exp Med 182: 1545–1556.
   PubMed Web of Science ®Google Scholar
• Mattson MP (2000). Apoptosis in neurodegenerative disor-ders. Nat Rev Mol Cell Biol 1: 120–129.
   PubMed Web of Science ®Google Scholar
• McGuire SO, Ling ZD, Lipton JW, Sortwell CE, Collier TJ, Carvey PM (2001). Tumor necrosis factor alpha is toxic to embryonic mesencephalic dopamine neurons. Exp Neurol 169: 219–230.
   PubMed Web of Science ®Google Scholar
• Nava VE, Rosen A, Veliuona MA, Clem RJ, Levine B, Hardwick JM (1998). Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. I Virol 72: 452–459.
   Google Scholar
• Nunez G, Benedict MA, Hu Y, Inohara N (1998). Caspases: The proteases of the apoptotic pathway. Oncogene 17: 3237–3245.
   Google Scholar
• Oberhaus SM, Smith RL, Clayton GH, Dermody TS, Tyler KL (1997). Reovirus infection and tissue injury in the mouse central nervous system are associated with apop-tosis. I Virol 71: 2100–2106.
   Google Scholar
• Ohagen A, Ghosh S, He J, Huang K, Chen Y, Yuan M, Osathanondh R, Gartner S, Shi B, Shaw G, Gabuzda D (1999). Apoptosis induced by infection of primary brain cultures with diverse human immunodeficiency virus type 1 isolates: Evidence for a role of the envelope. I Virol 73: 897–906.
   Google Scholar
• Patel CA, Mukhtar M, Pomerantz RJ (2000). Human im-munodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. I Virol 74: 9717–9726.
   PubMed Web of Science ®Google Scholar
• Pekosz A, Phillips J, Pleasure D, Merry D, Gonzalez-Scaran o F (1996). Induction of apoptosis by La Crosse virus in-fection and role of neuronal differentiation and human bc1-2 expression in its prevention. I Virol 70: 5329–5335.
   PubMedGoogle Scholar
• Petito CK, Kerza-Kwiatecki AP, Gendelman HE, McCarthy M, Nath A, Podack ER, Shapshak P, Wiley CA (1999). Review: Neuronal injury in HIV infection. I NeuroVirol 5: 327–341.
   PubMed Web of Science ®Google Scholar
• Pettersen RD (2000). CD47 and death signaling in the im-mune system. Apoptosis 5: 299–306.
   Google Scholar
• Poggioli GJ, Keefer C, Connolly JL, Dermody TS, Tyler KL (2000). Reovirus-induced G(2)/M cell cycle arrest re-quires sigma1s and occurs in the absence of apoptosis. I Virol 74: 9562–9570.
   PubMed Web of Science ®Google Scholar
• Raghupathi R, Graham DI, McIntosh TK (2000). Apopto-sis after traumatic brain injury. I Neurotrauma 17: 927–938.
   PubMed Web of Science ®Google Scholar
• Ray AM, Owen DE, Evans ML, Davis JB, Benham CD (2000). Caspase inhibitors are functionally neuroprotec - tive against oxygen glucose deprivation induced CA1 death in rat organotypic hippocampal slices. Brain Res 867: 62–69.
   Google Scholar
• Reed JC (2000). Mechanisms of apoptosis. Am J Pathol 157: 1415–1430.
   PubMed Web of Science ®Google Scholar
• Rentsch M, Beham A, Iesalnieks I, Mirwald T, Anthuber M, Jauch KW (2001). Impact of prolonged cold ischemia and reperfusion on apoptosis, activation of caspase 3, and expression of bax after liver transplantation in the rat. Transplant Proc 33: 850–851.
   PubMed Web of Science ®Google Scholar
• Rodgers SE, Barton ES, Oberhaus SM, Pike B, Gibson CA, Tyler KL, Dermody TS (1997). Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bc1-2. I Virol 71: 2540–2546.
   PubMed Web of Science ®Google Scholar
• Rosenbaum DM, Gupta G, D'Amore J, Singh M, Weidenheim K, Zhang H, Kessler JA (2000). Fas (CD95/ APO-1) plays a role in the pathophysiology of focal cere-bral ischemia. J Neurosci Res 61: 686–692.
   PubMed Web of Science ®Google Scholar
• Sporer B, Koedel U, Goebel FD, Pfister HW (2000). In-creased levels of soluble Fas receptor and Fas ligand in the cerebrospinal fluid of HIV-infected patients. AIDS Res Hum Retroviruses 16: 221–226.
   PubMedGoogle Scholar
• Strater J, Moller P (2000). Expression and function of death receptors and their natural ligands in the intestine. Ann N Y Acad Sci 915: 162–170.
   PubMed Web of Science ®Google Scholar
• Tan Z, Levid J, Schreiber SS (2001). Increased expression of Fas (CD95/AP0-1) in adult rat brain after kainate-induced seizures. Neuroreport 12: 1979–1982.
   Google Scholar
• Tepper CG, Seldin MF (1999). Modulation of caspase-8 and FLICE-inhibitory protein expression as a poten-tial mechanism of Epstein-Barr virus tumorigenesis in Burkitt's lymphoma. Blood 94: 1727–1737.
   PubMed Web of Science ®Google Scholar
• Thompson RL, Sawtell NM (2000). HSV latency-associated transcript and neuronal apoptosis. Science 289: 1651.
   PubMedGoogle Scholar
• Tyler KL (2001). Fileds virology: mammalian reoviruses, 4th ed. Knipe DM, Howley PM (eds). Lippincott-Williams & Wilkins: Philadelphia, PA.
   Google Scholar
• Tyler KL, Bronson RT, Byers KB, Fields B (1985). Molec-ular basis of viral neurotropism: experimental reovirus infection. Neurology 35: 88–92.
   Google Scholar
• Tyler KL, Squier MK, Rodgers SE, Schneider BE, Oberhaus SM, Grdina TA, Cohen JJ, Dermody TS (1995). Differ-ences in the capacity of reovirus strains to induce apop-tosis are determined by the viral attachment protein sigma 1.1 Virol 69: 6972–6979.
   Google Scholar
• Tyler KL, Virgin HW, Bassel-Duby R, Fields BN (1989). An-tibody inhibits defined stages in the pathogenesis of re-ovirus serotype 3 infection of the central nervous sys-tem. J Exp Med 170: 887–900.
   Google Scholar
• Velier JJ, Ellison JA, Kikly KK, Spera PA, Barone FC, Feuerstein GZ (1999). Caspase-8 and caspase-3 are ex-pressed by different populations of cortical neurons un-dergoing delayed cell death after focal stroke in the rat. J Neurosci 19: 5932–5941.
   PubMed Web of Science ®Google Scholar
• Virgin HW, Bassel-Duby R, Fields BN, Tyler KL (1988). An-tibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). I Virol 62: 4594–4604.
   Google Scholar
• Yuan J, Yankner BA (2000). Apoptosis in the nervous sys-tem. Nature 407: 802–809.
   PubMed Web of Science ®Google Scholar