HSV targeting of the host phosphatase PP1α is required for disseminated disease in the neonate and contributes to pathogenesis in the brain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 50, 2015, Pages E6937-E6944

  Wilcox, Douglas R ^a   Muller, William J ^a   Longnecker, Richard ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Disseminated disease; HSV 1; Interferon response; Translational arrest

Indexed keywords

INITIATION FACTOR 2ALPHA; INTERFERON; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1 ALPHA; UNCLASSIFIED DRUG; VIRUS PROTEIN; INITIATION FACTOR 2; PHOSPHOPROTEIN PHOSPHATASE;

ADULT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CYTOKINE RESPONSE; EX VIVO STUDY; FEMALE; HELA CELL LINE; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS 1; HOST RESISTANCE; HUMAN; HUMAN CELL; MOUSE; NEUROPATHOLOGY; NEWBORN; NEWBORN INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; SIGNAL TRANSDUCTION; VIRUS MUTANT; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; BRAIN DISEASE; HERPES SIMPLEX; IN VITRO STUDY; METABOLISM; PATHOGENICITY; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIMPLEXVIRUS; VIRULENCE;

ANIMALS; ANIMALS, NEWBORN; BRAIN DISEASES; EUKARYOTIC INITIATION FACTOR-2; HERPES SIMPLEX; IN VITRO TECHNIQUES; MICE; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; SIMPLEXVIRUS; VIRULENCE;

EID: 84950324040     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513045112     Document Type: Article

References (43)

1. Pinninti SG, Kimberlin DW (2013) Neonatal herpes simplex virus infections. Pediatr Clin North Am 60(2):351-365.
2. Kimberlin DW, et al.; National Institute of Allergy and Infectious Diseases Collaborative Antiviral Study Group (2001) Natural history of neonatal herpes simplex virus infections in the acyclovir era. Pediatrics 108(2):223-229.
3. Langenberg AG, Corey L, Ashley RL, Leong WP, Straus SE; Chiron HSV Vaccine Study Group (1999) A prospective study of new infections with herpes simplex virus type 1 and type 2. N Engl J Med 341(19):1432-1438.
4. Bernstein DI, et al. (2013) Epidemiology, clinical presentation, and antibody response to primary infection with herpes simplex virus type 1 and type 2 in young women. Clin Infect Dis 56(3):344-351.
5. Jones CA, Raynes-Greenow C, Isaacs D; Neonatal HSV Study Investigators and Contributors to the Australian Paediatric Surveillance Unit (2014) Population-based surveillance of neonatal herpes simplex virus infection in Australia, 1997-2011. Clin Infect Dis 59(4):525-531.
6. Chou J, Chen JJ, Gross M, Roizman B (1995) Association of a M (r) 90, 000 phosphoprotein with protein kinase PKR in cells exhibiting enhanced phosphorylation of translation initiation factor eIF-2 alpha and premature shutoff of protein synthesis after infection with gamma 134.5-mutants of herpes simplex virus 1. Proc Natl Acad Sci USA 92(23):10516-10520.
7. He B, Gross M, Roizman B (1997) The gamma (1) 34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 94(3):843-848.
8. Leib DA, Machalek MA, Williams BR, Silverman RH, Virgin HW (2000) Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci USA 97(11):6097-6101.
9. Cheng G, Gross M, Brett ME, He B (2001) AlaArg motif in the carboxyl terminus of the gamma (1) 34.5 protein of herpes simplex virus type 1 is required for the formation of a high-molecular-weight complex that dephosphorylates eIF-2alpha. J Virol 75(8):3666-3674.
10. Verpooten D, Ma Y, Hou S, Yan Z, He B (2009) Control of TANK-binding kinase 1-mediated signaling by the gamma (1) 34.5 protein of herpes simplex virus 1. J Biol Chem 284(2):1097-1105.
11. Orvedahl A, et al. (2007) HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1(1):23-35.
12. Tallóczy Z, et al. (2002) Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci USA 99(1):190-195.
13. Wilcox DR, Wadhwani NR, Longnecker R, Muller WJ (2015) Differential reliance on autophagy for protection from HSV encephalitis between newborns and adults. PLoS Pathog 11(1):e1004580.
14. Cheng G, Feng Z, He B (2005) Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2alpha dephosphorylation by the gamma (1) 34.5 protein. J Virol 79(3):1379-1388.
15. McGeoch DJ, Barnett BC (1991) Neurovirulence factor. Nature 353(6345):609.
16. He B, Chou J, Liebermann DA, Hoffman B, Roizman B (1996) The carboxyl terminus of the murine MyD116 gene substitutes for the corresponding domain of the gamma (1) 34.5 gene of herpes simplex virus to preclude the premature shutoff of total protein synthesis in infected human cells. J Virol 70(1):84-90.
17. Zhang C, et al. (2008) A conserved domain of herpes simplex virus ICP34.5 regulates protein phosphatase complex in mammalian cells. FEBS Lett 582(2):171-176.
18. Verpooten D, et al. (2009) Dephosphorylation of eIF2alpha mediated by the gamma134.5 protein of herpes simplex virus 1 facilitates viral neuroinvasion. J Virol 83(23):12626-12630.
19. Radtke K, et al. (2013) Inhibition of the host translation shutoff response by herpes simplex virus 1 triggers nuclear envelope-derived autophagy. J Virol 87(7):3990-3997.
20. Chou J, Roizman B (1992) The gamma 1(34.5) gene of herpes simplex virus 1 precludes neuroblastoma cells from triggering total shutoff of protein synthesis characteristic of programmed cell death in neuronal cells. Proc Natl Acad Sci USA 89(8):3266-3270.
21. Meurs E, et al. (1990) Molecular cloning and characterization of the human doublestranded RNA-activated protein kinase induced by interferon. Cell 62(2):379-390.
22. Balachandran S, et al. (2000) Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13(1):129-141.
23. Patel RC, Sen GC (1998) PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J 17(15):4379-4390.
24. Ito T, Yang M, May WS (1999) RAX, a cellular activator for double-stranded RNAdependent protein kinase during stress signaling. J Biol Chem 274(22):15427-15432.
25. Boyce M, et al. (2005) A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307(5711):935-939.
26. Bryant KF, et al. (2008) ICP34.5-dependent and -independent activities of salubrinal in herpes simplex virus-1 infected cells. Virology 379(2):197-204.
27. Chen SF, et al. (2004) Seizure, neuron loss, and mossy fiber sprouting in herpes simplex virus type 1-infected organotypic hippocampal cultures. Epilepsia 45(4):322-332.
28. Dionne KR, Leser JS, Lorenzen KA, Beckham JD, Tyler KL (2011) A brain slice culture model of viral encephalitis reveals an innate CNS cytokine response profile and the therapeutic potential of caspase inhibition. Exp Neurol 228(2):222-231.
29. Braun E, et al. (2006) Neurotropism of herpes simplex virus type 1 in brain organ cultures. J Gen Virol 87(Pt 10):2827-2837.
30. Bolovan CA, Sawtell NM, Thompson RL (1994) ICP34.5 mutants of herpes simplex virus type 1 strain 17syn+ are attenuated for neurovirulence in mice and for replication in confluent primary mouse embryo cell cultures. J Virol 68(1):48-55.
31. Chou J, Kern ER, Whitley RJ, Roizman B (1990) Mapping of herpes simplex virus-1 neurovirulence to gamma 134.5, a gene nonessential for growth in culture. Science 250(4985):1262-1266.
32. Kuma A, et al. (2004) The role of autophagy during the early neonatal starvation period. Nature 432(7020):1032-1036.
33. Siekierka J, Manne V, Ochoa S (1984) Mechanism of translational control by partial phosphorylation of the alpha subunit of eukaryotic initiation factor 2. Proc Natl Acad Sci USA 81(2):352-356.
34. Wek SA, Zhu S, Wek RC (1995) The histidyl-tRNA synthetase-related sequence in the eIF-2 alpha protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol Cell Biol 15(8):4497-4506.
35. Kollmann TR, Levy O, Montgomery RR, Goriely S (2012) Innate immune function by Toll-like receptors: Distinct responses in newborns and the elderly. Immunity 37(5):771-783.
36. Banisadr G, Podojil JR, Miller SD, Miller RJ (2015) Pattern of CXCR7 gene expression in mouse brain under normal and inflammatory conditions. J Neuroimmune Pharmacol PMID:25997895.
37. Mithal DS, Ren D, Miller RJ (2013) CXCR4 signaling regulates radial glial morphology and cell fate during embryonic spinal cord development. Glia 61(8):1288-1305.
38. Zheng LS, et al. (2014) Mechanisms for interferon-α-induced depression and neural stem cell dysfunction. Stem Cell Rep 3(1):73-84.
39. Rubovitch V, et al. (2015) The neuroprotective effect of salubrinal in a mouse model of traumatic brain injury. Neuromolecular Med 17(1):58-70.
40. Kimberlin DW, et al.; National Institute of Allergy and Infectious Diseases Collaborative Antiviral Study Group (2001) Safety and efficacy of high-dose intravenous acyclovir in the management of neonatal herpes simplex virus infections. Pediatrics 108(2):230-238.
41. Müller U, et al. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264(5167):1918-1921.
42. Adkins B, Leclerc C, Marshall-Clarke S (2004) Neonatal adaptive immunity comes of age. Nat Rev Immunol 4(7):553-564.
43. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37(2):173-182.