Home LiteratureArticle Details
PMID: 16912310 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with borna disease virus.

Journal of virology ·Vol. 80 ·No. 17 ·2006-09-00 ·Pages 8613-26

Williams BL, Lipkin WI

Abstract

Borna disease virus infection of neonatal rats results in a characteristic behavioral syndrome and apoptosis of subsets of neurons in the hippocampus and cerebellum (neonatal Borna disease [NBD]). The cellular mechanisms leading to neurodevelopmental damage in NBD have not been fully elucidated. Insights into this model may have general implications for understanding the pathogenesis of virus-associated neurodevelopmental damage. Here we report the presence of endoplasmic reticulum (ER) stress markers and activation of the unfolded protein response in the NBD hippocampus and cerebellum. Specific findings included enhanced PERK-mediated phosphorylation of eif2alpha and concomitant regulation of ATF4 translation; IRE1-mediated splicing of XBP1 mRNA; and cleavage of the ATF6 protein in NBD rat brains. We found evidence for regional and cell type-specific divergence in the expression of ER stress-induced proapoptotic and quality control signals. Our results demonstrate that ER stress induction in death-susceptible Purkinje neurons in NBD is associated with the expression of the proapoptotic molecule CHOP in the absence of compensatory expression of the ER quality control molecules Bip and protein disulfide isomerase. In contrast, ER stress in death-resistant astrocytes is associated with complementary expression of CHOP and ER quality control signals. These results implicate an imbalance between ER stress-mediated apoptosis and survival signaling as a critical determinant of neural cell fate in NBD.

MeSH Terms
Animals Animals, Newborn/virology Apoptosis Astrocytes/pathology Borna Disease/pathology,virology Borna disease virus/pathogenicity Cerebellum/metabolism,pathology,virology Endoplasmic Reticulum/pathology Female Gene Expression Regulation Heat-Shock Response Hippocampus/metabolism,pathology,virology Nerve Degeneration/pathology Neurons/pathology Oligonucleotide Array Sequence Analysis Protein Folding Proteins/genetics,metabolism Rats Rats, Inbred Lew
Chemicals
Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Williams B L
Jerome L. and Dawn Greene Infectious Disease Laboratory, Mailman School of Public Health, Columbia University, New York, NY 10032, USA. wil2001@columbia.edu
Lipkin W I
References (79)
79 references, click to expand
  1. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins.
    Nature. 1988 Mar 31;332(6163):462-4 PMID: 3352747
  2. Astrocytes and Schwann cells are virus-host cells in the nervous system of rats with Borna disease.
    J Neuropathol Exp Neurol. 1989 Nov;48(6):631-44 PMID: 2507750
  3. Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer.
    Biochemistry. 1991 Jan 22;30(3):613-9 PMID: 1988050
  4. CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest.
    Genes Dev. 1994 Feb 15;8(4):453-64 PMID: 8125258
  5. Genomic organization of Borna disease virus.
    Proc Natl Acad Sci U S A. 1994 May 10;91(10):4362-6 PMID: 8183914
  6. Molecular biology of borna disease virus: prototype of a new group of animal viruses.
    J Virol. 1994 Dec;68(12):7669-75 PMID: 7966555
  7. Enzyme-linked immunosorbent assay for detecting antibodies to Borna disease virus-specific proteins.
    J Clin Microbiol. 1995 Feb;33(2):348-51 PMID: 7714191
  8. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase.
    Science. 1996 May 31;272(5266):1347-9 PMID: 8650547
  9. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153).
    Mol Cell Biol. 1996 Aug;16(8):4273-80 PMID: 8754828
  10. Developmental injury to the cerebellum following perinatal Borna disease virus infection.
    Brain Res Dev Brain Res. 1995 Dec 21;90(1-2):45-53 PMID: 8719328
  11. Exposure of astrocytes to hypoxia/reoxygenation enhances expression of glucose-regulated protein 78 facilitating astrocyte release of the neuroprotective cytokine interleukin 6.
    J Neurochem. 1996 Mar;66(3):973-9 PMID: 8769856
  12. Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells.
    FEBS Lett. 1996 Oct 21;395(2-3):143-7 PMID: 8898082
  13. 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 U S A. 1997 Feb 4;94(3):843-8 PMID: 9023344
  14. Processing of the Borna disease virus glycoprotein gp94 by the subtilisin-like endoprotease furin.
    J Virol. 1998 May;72(5):4528-33 PMID: 9557754
  15. Evolution of the immune response in the central nervous system following infection with Borna disease virus.
    J Neuroimmunol. 1998 Oct 1;90(2):137-42 PMID: 9817441
  16. Comparative study of endoplasmic reticulum stress-induced neuronal death in rat cultured hippocampal and cerebellar granule neurons.
    Neurochem Int. 2006 Aug;49(3):285-93 PMID: 16545889
  17. Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP.
    Nat Genet. 2005 Sep;37(9):974-9 PMID: 16116427
  18. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress.
    Mol Biol Cell. 1999 Nov;10(11):3787-99 PMID: 10564271
  19. Effects of neonatal rat Borna disease virus (BDV) infection on the postnatal development of the brain monoaminergic systems.
    Brain Res Dev Brain Res. 2000 Feb 7;119(2):179-85 PMID: 10675767
  20. Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death.
    J Biol Chem. 2000 Apr 7;275(14):10388-93 PMID: 10744727
  21. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats.
    Brain Pathol. 2000 Apr;10(2):260-72 PMID: 10764045
  22. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response.
    Nat Cell Biol. 2000 Jun;2(6):326-32 PMID: 10854322
  23. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells.
    Diabetes. 2005 Feb;54(2):452-61 PMID: 15677503
  24. Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons.
    J Cereb Blood Flow Metab. 2005 Jan;25(1):41-53 PMID: 15678111
  25. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes.
    Nat Cell Biol. 2005 Feb;7(2):186-94 PMID: 15665855
  26. Human cytomegalovirus protein US11 provokes an unfolded protein response that may facilitate the degradation of class I major histocompatibility complex products.
    J Virol. 2005 Mar;79(5):2768-79 PMID: 15708995
  27. Tula hantavirus triggers pro-apoptotic signals of ER stress in Vero E6 cells.
    Virology. 2005 Mar 1;333(1):180-9 PMID: 15708603
  28. Endoplasmic reticulum calcium signaling in nerve cells.
    Biol Res. 2004;37(4):693-9 PMID: 15709699
  29. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress.
    Methods. 2005 Apr;35(4):373-81 PMID: 15804610
  30. Human cytomegalovirus infection activates and regulates the unfolded protein response.
    J Virol. 2005 Jun;79(11):6890-9 PMID: 15890928
  31. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1.
    Mol Cell Biol. 2000 Jul;20(14):5096-106 PMID: 10866666
  32. Depletion of intracellular Ca2+ by caffeine and ryanodine induces apoptosis of chinese hamster ovary cells transfected with ryanodine receptor.
    J Biol Chem. 2000 Jun 30;275(26):19978-84 PMID: 10764805
  33. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response.
    Mol Cell Biol. 2000 Sep;20(18):6755-67 PMID: 10958673
  34. An endoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of A549 epithelial cells by respiratory syncytial virus.
    J Cell Biochem. 2001;80(3):441-54 PMID: 11135374
  35. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state.
    Mol Cell Biol. 2001 Feb;21(4):1249-59 PMID: 11158311
  36. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs.
    Mol Cell. 2000 Dec;6(6):1355-64 PMID: 11163209
  37. Stress-inducible transcription factor CHOP/gadd153 induces apoptosis in mammalian cells via p38 kinase-dependent and -independent mechanisms.
    Exp Cell Res. 2001 Jul 15;267(2):193-204 PMID: 11426938
  38. Translational control is required for the unfolded protein response and in vivo glucose homeostasis.
    Mol Cell. 2001 Jun;7(6):1165-76 PMID: 11430820
  39. Borna disease: virus-induced neurobehavioral disease pathogenesis.
    Curr Opin Microbiol. 2001 Aug;4(4):467-75 PMID: 11495813
  40. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor.
    Cell. 2001 Dec 28;107(7):881-91 PMID: 11779464
  41. Regulated translation initiation controls stress-induced gene expression in mammalian cells.
    Mol Cell. 2000 Nov;6(5):1099-108 PMID: 11106749
  42. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors.
    J Biol Chem. 1998 Dec 11;273(50):33741-9 PMID: 9837962
  43. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase.
    Nature. 1999 Jan 21;397(6716):271-4 PMID: 9930704
  44. Ca2+ regulation of interactions between endoplasmic reticulum chaperones.
    J Biol Chem. 1999 Mar 5;274(10):6203-11 PMID: 10037706
  45. Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein.
    J Virol. 1999 May;73(5):3718-22 PMID: 10196264
  46. Cytokine expression in the rat central nervous system following perinatal Borna disease virus infection.
    J Neuroimmunol. 1999 Apr 1;96(1):29-45 PMID: 10227422
  47. Persistent Borna disease virus infection of neonatal rats causes brain regional changes of mRNAs for cytokines, cytokine receptor components and neuropeptides.
    Brain Res Bull. 1999 Aug;49(6):441-51 PMID: 10483922
  48. An infection-based model of neurodevelopmental damage.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12102-7 PMID: 10518583
  49. ER stress and the unfolded protein response.
    Mutat Res. 2005 Jan 6;569(1-2):29-63 PMID: 15603751
  50. Minor folding defects trigger local modification of glycoproteins by the ER folding sensor GT.
    EMBO J. 2005 May 4;24(9):1730-8 PMID: 15861139
  51. The protective effect of dantrolene on ischemic neuronal cell death is associated with reduced expression of endoplasmic reticulum stress markers.
    Brain Res. 2005 Jun 28;1048(1-2):59-68 PMID: 15921666
  52. Endoplasmic reticulum quality control and apoptosis.
    Acta Biochim Pol. 2005;52(2):381-95 PMID: 15933766
  53. Maturation of Borna disease virus glycoprotein.
    FEBS Lett. 2005 Aug 29;579(21):4751-6 PMID: 16098520
  54. ER stress and neurodegenerative diseases.
    Cell Death Differ. 2006 Mar;13(3):385-92 PMID: 16397584
  55. Emergence of endoplasmic reticulum stress and activated microglia in Purkinje cell degeneration mice.
    Neurosci Lett. 2006 Mar 27;396(2):91-6 PMID: 16356646
  56. Astrocytes survive chronic infection and cytopathic effects of the ts1 mutant of the retrovirus Moloney murine leukemia virus by upregulation of antioxidant defenses.
    J Virol. 2006 Apr;80(7):3273-84 PMID: 16537594
  57. Metallothioneins and zinc dysregulation contribute to neurodevelopmental damage in a model of perinatal viral infection.
    Brain Pathol. 2006 Jan;16(1):1-14 PMID: 16612977
  58. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response.
    J Virol. 2002 May;76(9):4162-71 PMID: 11932381
  59. Why do Purkinje cells die so easily after global brain ischemia? Aldolase C, EAAT4, and the cerebellar contribution to posthypoxic myoclonus.
    Adv Neurol. 2002;89:331-59 PMID: 11968459
  60. Coordination of ATF6-mediated transcription and ATF6 degradation by a domain that is shared with the viral transcription factor, VP16.
    J Biol Chem. 2002 Jun 7;277(23):20734-9 PMID: 11909875
  61. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway.
    J Virol. 2002 Aug;76(15):7453-9 PMID: 12097557
  62. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals.
    Dev Cell. 2002 Jul;3(1):99-111 PMID: 12110171
  63. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response.
    Biochem J. 2002 Sep 1;366(Pt 2):585-94 PMID: 12014989
  64. Tumor necrosis factor induces apoptosis in hepatoma cells by increasing Ca(2+) release from the endoplasmic reticulum and suppressing Bcl-2 expression.
    J Biol Chem. 2002 Aug 30;277(35):31381-9 PMID: 12077131
  65. Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells.
    J Virol. 2002 Oct;76(19):9588-99 PMID: 12208938
  66. Loading neurons with BAPTA-AM activates xbp1 processing indicative of induction of endoplasmic reticulum stress.
    Cell Calcium. 2003 Feb;33(2):83-9 PMID: 12531184
  67. Protein synthesis and endoplasmic reticulum stress can be modulated by the hepatitis C virus envelope protein E2 through the eukaryotic initiation factor 2alpha kinase PERK.
    J Virol. 2003 Mar;77(6):3578-85 PMID: 12610133
  68. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress.
    Mol Cell. 2003 Mar;11(3):619-33 PMID: 12667446
  69. Dysregulated ryanodine receptors mediate cellular toxicity: restoration of normal phenotype by FKBP12.6.
    J Biol Chem. 2003 Aug 1;278(31):28856-64 PMID: 12754204
  70. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway.
    J Cell Biol. 2003 Aug 18;162(4):587-97 PMID: 12913114
  71. Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements.
    J Biol Chem. 2003 Sep 26;278(39):37375-85 PMID: 12871976
  72. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response.
    Mol Cell Biol. 2003 Nov;23(21):7448-59 PMID: 14559994
  73. Endoplasmic reticulum stress is a determinant of retrovirus-induced spongiform neurodegeneration.
    J Virol. 2003 Dec;77(23):12617-29 PMID: 14610184
  74. ORP150/HSP12A regulates Purkinje cell survival: a role for endoplasmic reticulum stress in cerebellar development.
    J Neurosci. 2004 Feb 11;24(6):1486-96 PMID: 14960622
  75. Roles of CHOP/GADD153 in endoplasmic reticulum stress.
    Cell Death Differ. 2004 Apr;11(4):381-9 PMID: 14685163
  76. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response.
    J Biol Chem. 2004 Apr 23;279(17):17158-64 PMID: 14960590
  77. Activation of endoplasmic reticulum stress signaling pathway is associated with neuronal degeneration in MoMuLV-ts1-induced spongiform encephalomyelopathy.
    Lab Invest. 2004 Jul;84(7):816-27 PMID: 15094714
  78. Endoplasmic reticulum (ER) stress induced by a neurovirulent mouse retrovirus is associated with prolonged BiP binding and retention of a viral protein in the ER.
    J Biol Chem. 2004 Aug 6;279(32):33782-90 PMID: 15178688
  79. Behavioral disease in rats caused by immunopathological responses to persistent borna virus in the brain.
    Science. 1983 Jun 24;220(4604):1401-3 PMID: 6602380
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2006-09-00
Pages
8613-26
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1563873
Subset
IM
Grants
NICHD NIH HHS · R01 HD037546 · United States
NICHD NIH HHS · HD37546 · United States
NINDS NIH HHS · NS29425 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com