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Extracellular HSP70, Neuroinflammation and Protection Against Viral Virulence

  • Michael OglesbeeEmail author
  • Mi Young Kim
  • Yaoling Shu
  • Sonia Longhi
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 16)

Abstract

The major inducible 70 kDa heat shock protein (hsp70) is induced by and supports intracellular replication of viruses belonging to diverse families. Paradoxically, this virus-hsp70 interaction is protective in mouse models of viral neurovirulence, enhancing T cell mediated immune clearance in an interferon β (IFN-β)-dependent manner. Protection reflects early release of hsp70 from viable infected neurons and induction of strong innate immune responses in uninfected brain macrophages, including the induction of IFN-β through Toll-like receptor 4. Potency of the response is inherent in the fact that hsp70 is released at a time when pathogen-associated molecular patterns (PAMPs) are in low abundance, and that the innate response is driven by uninfected cells, free from viral interference. Release of hsp70 from viable cells is primarily exosomal, and infection enhances total exosome release and hsp70 content on the surface of exosomes. Exosome content of hsp70 reflects levels of hsp70 in the infected cell. Findings have broad virological relevance and support a protective role for fever, a potent stimulus for hsp70 induction. While protective in the context of microbial infection, recent findings support potential untoward effects of inappropriate extracellular hsp70 release in non-infectious neuroinflammatory conditions.

Keywords

70 kDa heat shock protein Exosome Hsp70 Interferon beta Neurovirulence Virus clearance 

Abbreviations

ANOVA

Analysis of variance

CHUK

Conserved helix-loop-helix ubiquitous ligase

CNS

Central nervous system

CSF

Cerebrospinal fluid

DAMP

Damage-associated molecular pattern

DMEM

Dulbecco’s Modified Eagle medium

Ed CAM/RB

Rodent brain adapted Ed-MeV

Ed-MeV

Edmonston measles virus

ELISA

Enzyme-linked immunosorbent assay

FCS

Fetal calf serum

H-2

Mouse major histocompatibility complex

HSF

Heat shock factor

hsp70

70 kDa heat shock protein

IFN

Interferon

IFNAR

Type 1 interferon receptor

ILV

Intralumenal vesicle

IRF3

Interferon regulatory factor 3

L

Viral polymerase protein

LDH

Lactate dehydrogenase

LPS

Lipopolysaccharide

MEF

Mouse embryo fibroblasts

MeV

Measles virus

MHC

Major histocompatibility complex

MVB

Multivesicular body

N

Nucleocapsid protein

N2a-HSP

Mouse neuroblastoma cells that constitutively express hsp70

N2a-V

Vector transfected control mouse neuroblastoma cells

NBD

Nucleotide binding domain

NDV

Newcastle disease virus

NSE

Neuron specific enolase

NTAIL

Carboxyl terminus of the N protein

PAMP

Pathogen-associated molecular pattern

PBD

Peptide binding domain (also known as the substrate binding domain, SBD)

RSV

Respiratory syncytial virus

RT-PCR

Reverse transcription polymerase chain reaction

SBD

Substrate binding domain

STAT-1

Signal transducer and activator of transcription 1

TLR

Toll-like receptor

TRAM

Toll-like receptor adapter molecule 2

TRIF

TIR-domain-containing adapter-inducing interferon-β

VSV

Vesicular stomatitis virus

Notes

Acknowledgements

This work was supported in part by funds from the National Institute of Neurological Disorders and Stroke (R01NS31693). We thank Dr. Mamuka Kvaratskhelia (The Ohio State University) for assistance in the proteome analysis of exosomes and Dr. Prosper Boyaka (The Ohio State University) for suggestions in preparing the manuscript.

References

  1. Anand PK (2010) Exosomal membrane molecules are potent immune response modulators. Commun Integr Biol 3:405–408PubMedPubMedCentralCrossRefGoogle Scholar
  2. Anand PK, Anand E, Bleck CK, Anes E, Griffiths G (2010) Exosomal Hsp70 induces a pro-inflammatory response to foreign particles including mycobacteria. PLoS One 5:e10136PubMedPubMedCentralCrossRefGoogle Scholar
  3. Awad H, Suntres Z, Heijmans J, Smeak D, Bergdall-Costell V, Cristofi FL, Magro C, Oglesbee M (2008) Intracellular and extracellular expression of the major inducible 70 kDa heat shock protein in experimental ischemia-reperfusion injury of the spinal cord. Exp Neurol 212:275–284PubMedCrossRefPubMedCentralGoogle Scholar
  4. Basu S, Binder R, Suto R, Anderson K, Srivastava P (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol 12(11):1539–1546PubMedCrossRefGoogle Scholar
  5. Beauvillain C, Donnou S, Jarry U, Scotet M, Gascan H, Delneste Y, Guermonprez P, Jeannin P, Couez D (2008) Neonatal and adult microglia cross-present exogenous antigens. Glia 56:69–77PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bellini W, Rota J, Lowe L, Katz R, Dyken P, Zaki S, Shieh W, Rota P (2005) Subacute sclerosing panencephalitis: more cases of this fatal disease are prevented by measles immunization than was previously recognized. J Infect Dis 192(10):1686–1693PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bitnum A, Shannon P, Durward A, Rota P, Bellini W, Graham C, Wang E, Ford-Jones E, Cox P, Becker L, Fearon M, Petric M, Tellier R (1999) Measles inclusion body encephalitis caused by the vaccine strain of measles virus. Clin Infect Dis 29(4):855–861CrossRefGoogle Scholar
  8. Blixenkrone-Moller M, Bernard A, Bencsik A, Sixt N, Diamond L, Logan J, Wild T (1998) Role of CD46 in measles virus infection in CD46 transgenic mice. Virology 249:238–248PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bourhis JM, Receveur-Bréchot V, Oglesbee M, Zhang X, Buccellato M, Darbon H, Canard B, Finet S, Longhi S (2005) The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci 14:1975–1992PubMedPubMedCentralCrossRefGoogle Scholar
  10. Brasier A, Spratt H, Wu Z, Boldogh I, Zhang Y, Garofalo R, Casola A, Pashmi J, Haag A, Luxon B, Kurosky A (2004) Nuclear heat shock response and novel nulear domain 10 reorganization in respiratory syncytial virus-infected A549 cells identified by high-resolution two-dimensional gel electrophoresis. J Virol 21:11461–11476CrossRefGoogle Scholar
  11. Brooks G, Butel J, Morse S (1998) Paramyxovirus and rubella virus. In: Butler J, Ransom J, Ryan E (eds) Adelberg’s microbiology. Appleton and Lange, Stanford, pp 507–527Google Scholar
  12. Brown G, Rixon H, Steel J, McDonald T, Pitt A, Graham S, Sugrue R (2005) Evidence for an association between heat shock protein 70 and the respiratory syncytial virus polymerase complex within lipid-raft membranes during virus infection. Virology 338:69–80PubMedCrossRefPubMedCentralGoogle Scholar
  13. Carsillo T, Carsillo M, Niewiesk S, Vasconcelos D, Oglesbee M (2004) Hyperthermic preconditioning promotes measles virus clearance from brain in a mouse model of persistent infection. Brain Res 1004:73–82PubMedCrossRefPubMedCentralGoogle Scholar
  14. Carsillo T, Zhang X, Vasconcelos D, Niewiesk S, Oglesbee M (2006) A single codon in the nucleocapsid protein C terminus contributes to in vitro and in vivo fitness of Edmonston measles virus. J Virol 80(6):2904–2912PubMedPubMedCentralCrossRefGoogle Scholar
  15. Carsillo T, Traylor Z, Choi C, Niewiesk S, Oglesbee M (2006a) Hsp72, a host determinant of measles virus neurovirulence. J Virol 80:11031–11039PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carsillo T, Zhang X, Vasconcelos D, Niewiesk S, Oglesbee M (2006b) A single codon in the nucleocapsid protein C terminus contributes to in vitro and in vivo fitness of Edmonston measles virus. J Virol 80:2904–2912PubMedPubMedCentralCrossRefGoogle Scholar
  17. Carsillo T, Carsillo M, Traylor Z, Rajala-Schultz P, Popovich P, Niewiesk S, Oglesbee M (2009) Major histocompatibility phenotype determines hsp70-dependent protection against measles virus neurovirulence. J Virol 83(11):5544–5555PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chen W, Lin Y, Liao C, Hsieh S (2000) Modulatory effects of the human heat shock protein 70 on DNA vaccination. J Biomed Sci 7:412–419PubMedCrossRefPubMedCentralGoogle Scholar
  19. Chen S, Bawa D, Besshoh S, Gurd JW, Brown IR (2005) Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain. J Neurosci Res 81:522–529PubMedCrossRefPubMedCentralGoogle Scholar
  20. Couturier M, Buccellato M, Costanzo S, Bourhis J, Shu Y, Nicaise M, Desmadril M, Flaudrops C, Longhi S, Oglesbee M (2010) High affinity binding between Hsp70 and the C-terminal domain of the measles virus nucleoprotein requires an Hsp40 co-chaperone. J Mol Recognit 23:301–315PubMedPubMedCentralGoogle Scholar
  21. Danzer KM, Ruf WP, Putcha P, Joyner D, Hashimoto T, Glabe C, Hyman BT, McLean PJ (2011) Heat-shock protein 70 modulates toxic extracellular alpha-synuclein oligomers and rescues trans-synaptic toxicity. FASEB J 25:326–336PubMedPubMedCentralCrossRefGoogle Scholar
  22. Das S, Laxminarayana S, Chandra N, Ravi V, Desai A (2009) Heat shock protein 70 on Neuro2a cells is a putative receptor for Japanese encephalitis virus. Virology 385(1):47–57PubMedCrossRefPubMedCentralGoogle Scholar
  23. Daugaard M, Rohde M, Jäättelä M (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710PubMedCrossRefPubMedCentralGoogle Scholar
  24. De Maio A (2011) Extracellular heat shock proteins, cellular export vesicles, and the Stress Observation System: a form of communication during injury, infection, and cell damage. It is never known how far a controversial finding will go! Dedicated to Ferruccio Ritossa. Cell Stress Chaperones 16:235–249PubMedCrossRefPubMedCentralGoogle Scholar
  25. Detje C, Meyer T, Schmidt H, Kruez D, Rose J, Bechmann I, Prinz M, Kalinke U (2009) Local type 1 IFN receptor signaling protects against virus spread within the central nervous system. J Immunol 182:2297–2304PubMedCrossRefPubMedCentralGoogle Scholar
  26. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, Whitten-Bauer C, Wieland S, Chisari FV (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12:558–570PubMedPubMedCentralCrossRefGoogle Scholar
  27. Duib-Jalbut S, Xia J, Rangaviggula H, Fang Y, Lee T (1999) Failure of measles virus to activate nuclear factor-κB in neuronal cells: implications on the immune response to viral infections in the central nervous system. J Immunol 162:4024–4029Google Scholar
  28. Finke D, Liebert U (1994) CD4(+) T cells are essential in overcoming experimental measles encephalitis. Immunology 83:184–189PubMedPubMedCentralGoogle Scholar
  29. Finke D, Brinckmann U, ter Meulen V, Liebert U (1995) Gamma interferon is a major mediator of antiviral defense in experimental measles virus-induced encephalitis. J Virol 69:5469–5474PubMedPubMedCentralGoogle Scholar
  30. Freeman BC, Myers MP, Schumacher R, Morimoto RI (1995) Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J 14:2281–2292PubMedPubMedCentralCrossRefGoogle Scholar
  31. Frühbeis C, Fröhlich D, Krämer-Albers EM (2012) Emerging roles of exosomes in neuron-glia communication. Front Physiol 3:119PubMedPubMedCentralCrossRefGoogle Scholar
  32. Glaser K, Hagos B, Molestina R (2011) Effects of Toxoplasma gondii genotype and absence of host MAL/Myd88 on the temporal regulation of gene expression in infected microglial cells. Exp Parasitol 129:409–413PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hecker J, Sundram H, Zou S, Praestgaard A, Bavaria J, Ramchandren S, McGarvey M (2008) Heat shock proteins HSP70 and HSP27 in the cerebrospinal fluid of patients undergoing thoracic aneurysm repair correlate with the probability of postoperative paralysis. Cell Stress Chaperones 13:435–446PubMedPubMedCentralCrossRefGoogle Scholar
  34. Henn A, Lund S, Hedtjarn M, Schrattenholz A, Porzgen P, Leist M (2009) The suitability of BV2 cells as alternative model system for primary microglia cultures or for animal experiments examining brain inflammation. ALTEX 26:83–94PubMedCrossRefGoogle Scholar
  35. Hofman F, Hinton D, Baemayr J, Weil M, Merrill J (1991) Lymphokines and immunoregulatory molecules in subacute sclerosing panencephalitis. Clin Immunol Immunopathol 58(3):331–342PubMedCrossRefGoogle Scholar
  36. Joncas J, Robillard L, Boudreault A, Leyritz M, McLaughlin B (1976) Letter: interferon in serum and cebrospinal fluid in subacute sclerosing panencephalitis. Can Med Assoc 115(4):309Google Scholar
  37. Kakimura J, Kitamura Y, Takata K, Umeki M, Suzuki S, Shibagaki K, Taniguchi T, Nomura Y, Gebicke-Haerter P, Smith M, Perry G, Shimohama S (2002) Microglial activation and amyloid-beta clearance induced by exogenous heat-shock proteins. FASEB J 16:601–603PubMedCrossRefGoogle Scholar
  38. Kallfass C, Ackerman A, Lienenklaus S, Weiss S, Heimrich B, Staeheli P (2012) Visualizing production of Beta interferon by astrocytes and microglia in brain of la crosse virus-infected mice. J Virol 86:11223–11230PubMedPubMedCentralCrossRefGoogle Scholar
  39. Katayama Y, Hotta H, Nishimura A (1995) Detection of measles virus nucleoprotein mRNA in autopsied brain tissues. J Gen Virol 76(Pt 12):3201–3204PubMedCrossRefGoogle Scholar
  40. Katayama Y, Kosho K, Nichimura A, Tatsuno Y, Homma M, Hotta H (1998) Detection of measles virus mRNA from autopsied human tissues. J Clin Microbiol 36(1):299–301PubMedPubMedCentralGoogle Scholar
  41. Katz M (1995) Clinical spectrum of measles. Curr Top Microbiol Immunol 191:1–12PubMedGoogle Scholar
  42. Kawanokuchi J, Mizuno T, Takeuchi H, Kato H, Wang J, Mitsuma N, Suzumura A (2006) Production of interferon gamma by microglia. Mult Scler 12(5):558–564PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kim MY, Shu Y, Carsillo T, Zhang J, Yu L, Peterson C, Longhi S, Girod S, Niewiesk S, Oglesbee M (2013a) Hsp70 and a novel axis of type 1 interferon-dependent antiviral immunity in the measles virus-infected brain. J Virol 87(2):998–1009PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kim MY, Ma Y, Zhang Y, Li J, Shu Y, Oglesbee M (2013b) hsp70-dependent antiviral immunity against cytopathic neuronal infection by vesicular stomatitis virus. J Virol 87(19):10668–10678PubMedPubMedCentralCrossRefGoogle Scholar
  45. Krakowka S (1989) Canine distemper virus infectivity of various blood fractions for central nervous system vasculature. J Neuroimmunol 21:75–80PubMedCrossRefGoogle Scholar
  46. Lahaye X, Vidy A, Fouquet B, Blondel D (2012) Hsp70 protein positively regulates rabies virus infection. J Virol 86(9):4743–4751PubMedPubMedCentralCrossRefGoogle Scholar
  47. Lancaster GI, Febbraio MA (2005) Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem 280:23349–23355PubMedCrossRefGoogle Scholar
  48. Letchworth G, Rodriguez L, Del cbarrera J (1999) Vesicular stomatitis. Vet J 157:239–260PubMedCrossRefGoogle Scholar
  49. Lieutaud P, Canard B, Longhi S (2008) MeDor: a metaserver for predicting protein disorder. BMC Genomics 9(Suppl 2):S25PubMedPubMedCentralCrossRefGoogle Scholar
  50. Liu Q, Hendrickson WA (2007) Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131:106–120PubMedPubMedCentralCrossRefGoogle Scholar
  51. Longhi S, Oglesbee M (2010) Structural disorder within the measles virus nucleoprotein and phosphoprotein. Protein Pept Lett 17(8):961–978PubMedCrossRefPubMedCentralGoogle Scholar
  52. Louveau A, Smirnov I, Keyes T, Eccles J, Rouhani S, Peske D, Derecki N, Castle D, Mandell J, Lee K, Harris T, Kipnis J (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560):337–341PubMedPubMedCentralCrossRefGoogle Scholar
  53. Luong M, Zhang Y, Chamberlain T, Zhou T, Wright J, Dower K, Hall JP (2012) Stimulation of TLR4 by recombinant HSP70 requires structural integrity of the HSP70 protein itself. J Inflamm 9:11CrossRefGoogle Scholar
  54. Macejak D, Sarnow P (1992) Association of heat shock protein 70 with enterovirus capsid precursor P1 in infected human cells. J Virol 66:1520–1527PubMedPubMedCentralGoogle Scholar
  55. Madara J, Krewet J, Shah M (2005) Heat shock protein 72 expression allows permissive replication of oncolytic adenovirus dl1520 (ONYX-015) in rat glioblastoma cells. Mol Cancer 4:12PubMedPubMedCentralCrossRefGoogle Scholar
  56. Marini A, Kozuka M, Lipsky R, Nowak T (1990) 70-kilodalton heat shock protein induction in cerebellar astrocytes and cerebellar granule cells in vitro: comparison with immunocytochemical localization after hyperthermia in vivo. J Neurochem 54:1509–1516PubMedCrossRefPubMedCentralGoogle Scholar
  57. Mayer M (2005) Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev Physiol Biochem Pharmacol 153:1–46PubMedCrossRefPubMedCentralGoogle Scholar
  58. Meckes DG, Raab-Traub N (2011) Microvesicles and viral infection. J Virol 85:12844–12854PubMedPubMedCentralCrossRefGoogle Scholar
  59. Moehler M, Zeidler M, Schede J, Rommelaere J, Galle P, Cornelis J, Heike M (2003) Oncolytic parvovirus H1 induces release of heat shock protein HSP72 in susceptible human tumor cells but may not affect primary immune cells. Cancer Gene Ther 10:477–480PubMedCrossRefGoogle Scholar
  60. Moore S, Kim MY, Maiolini A, Tipold A, Oglesbee M (2012) Extracellular hsp70 release in canine steroid responsive meningitis-arteritis. Vet Immunol Immunopathol 145(1–2):129–133PubMedCrossRefPubMedCentralGoogle Scholar
  61. Morrison-Bogorad M, Zimmerman A, Pardue S (1995) Heat shock 70 messenger RNA levels in human brain: correlation with agonal fever. J Neurochem 64:235–246PubMedCrossRefPubMedCentralGoogle Scholar
  62. Munday D, Wu W, Smith N, Fix J, Noton S, Galloux M, Touzelet O, Armstrong S, Dawson J, Aljabr W, Easton A, Rameix-Welti MA, de Oliveira A, Simabuco F, Ventura A, Hughes D, Barr J, Fearns R, Digard P, Eléouët JF, Hiscox J (2015) Interactome analysis of the human respiratory syncytial virus RNA polymerase complex identifies protein chaperones as important cofactors that promote L-protein stability and RNA synthesis. J Virol 89(2):917–930PubMedCrossRefPubMedCentralGoogle Scholar
  63. Nagy P, Wang R, Pogany J, Hafren A, Makinen K (2011) Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology 411:374–382PubMedCrossRefPubMedCentralGoogle Scholar
  64. Neumeister C, Niewiesk S (1998) Recognition of measles virus-infected cells by CD8+ T cells dependent upon the H-2 molecule. J Gen Virol 79:2583–2591PubMedCrossRefPubMedCentralGoogle Scholar
  65. Niewiesk S, Brinckmann U, Bankamp B, Sirak S, Liebert U, ter Meulen V (1993) Susceptibility to measles virus-induced encephalitis in mice correlates with impaired antigen presentation to cytotoxic lymphocytes. J Virol 67:75–81PubMedPubMedCentralGoogle Scholar
  66. Noessner E, Gastpar R, Milani V, Brandl A, Hutzler P, Kuppner M, Roos M, Kremmer E, Asea A, Calderwood S, Issels R (2002) Tumor derived heat shock protein complexes are cross-presented by human dendritic cells. J Immunol 169(10):5424–5432PubMedCrossRefGoogle Scholar
  67. Nozawa N, Yamauchi Y, Ohtsuka K, Kawaguchi Y, Nishiyama Y (2004) Formation of aggresome-like structures in herpes simplex virus type 2-infected cells and a potential role in virus assembly. Exp Cell Res 299(2):486–497PubMedCrossRefPubMedCentralGoogle Scholar
  68. Oglesbee M (2007) Nucleocapsid protein interactions with the major inducible 70 kDa heat shock protein. In: Longhi S (ed) Measles virus nucleoprotein. Nova Science Publishers, Hauppauge, pp 53–98Google Scholar
  69. Oglesbee M, Krakowka S (1993) The cellular stress response induces selective intranuclear trafficking and accumulation of morbillivirus major core protein. Lab Investig 68(1):109–117PubMedPubMedCentralGoogle Scholar
  70. Oglesbee M, Niewiesk S (2011) Measles virus neurovirulence and host immunity. Future Virol 6(1):85–99PubMedPubMedCentralCrossRefGoogle Scholar
  71. Oglesbee M, Tatalick L, Rice J, Krakowka S (1989) Isolation and characterization of canine distemper virus nucleocapsid variants. J Gen Virol 70:2409–2419PubMedCrossRefPubMedCentralGoogle Scholar
  72. Oglesbee M, Ringler S, Krakowka S (1990) Interaction of canine distemper virus nucleocapsid variants with 70 kDa heat shock proteins. J Gen Virol 71:1585–1590PubMedCrossRefPubMedCentralGoogle Scholar
  73. Oglesbee M, Kenney H, Kenney T, Krakowka S (1993) Enhanced production of morbillivirus gene-specific RNAs following induction of the cellular stress response in stable persistent infection. Virology 192:556–567PubMedCrossRefPubMedCentralGoogle Scholar
  74. Oglesbee M, Liu Z, Kenney H, Brooks C (1996) The highly inducible member of the 70 kDa family of heat shock proteins increases canine distemper virus polymerase activity. J Gen Virol 77:2125–2135PubMedCrossRefPubMedCentralGoogle Scholar
  75. Oglesbee M, Pratt M, Carsillo T (2002) Role for heat shock proteins in the immune response to measles virus infection. Viral Immunol 15:399–416PubMedCrossRefPubMedCentralGoogle Scholar
  76. Pack C, Kumaraguru U, Suvas S, Rouse B (2005) Heat-shock protein 70 acts as an effective adjuvant in neonatal mice and confers protection against challenge with herpes simplex virus. Vaccine 23:3526–3534PubMedCrossRefPubMedCentralGoogle Scholar
  77. Pardue S, Wang S, Miller M, Morrison-Bogorad M (2007) Elevated levels of inducible heat shock 70 proteins in human brain. Neurobiol Aging 28(2):314–324PubMedCrossRefPubMedCentralGoogle Scholar
  78. Patterson CE, Daley JK, Rall GF (2002a) Neuronal survival strategies in the face of RNA viral infection. J Infect Dis 186(Suppl 2):S215–S219PubMedCrossRefPubMedCentralGoogle Scholar
  79. Patterson CE, Lawrence DM, Echols LA, Rall G (2002b) Immune mediated protection from measles virus-induced central nervous system disease is non-cytolytic and γ interferon dependent. J Virol 76:4497–4506PubMedPubMedCentralCrossRefGoogle Scholar
  80. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A 107:6328–6333PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pien G, Nguyen K, Malmgaard L, Satoskar A, Biron C (2002) A unique mechanism for innate cytokine promotion of T cell responses to viral infections. J Immunol 169:5827–5837PubMedCrossRefPubMedCentralGoogle Scholar
  82. Qin H, Wilson C, Lee S, Zhao X, Benveniste E (2005) LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1alpha in macrophages and microglia. Blood 106:3114–3122PubMedPubMedCentralCrossRefGoogle Scholar
  83. Ran R, Zhou G, Lu A, Zhang L, Tang Y, Rigby AC, Sharp FR (2004) Hsp70 mutant proteins modulate additional apoptotic pathways and improve cell survival. Cell Stress Chaperones 9:229–242PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ren X, Xue C, Kong Q, Zhang C, Bi Y, Cao Y (2012) Proteomic analysis of purified Newcastle disease virus particles. Proteome Sci 10:32PubMedPubMedCentralCrossRefGoogle Scholar
  85. Rogers C, Fernandes-Alnemri T, Mayes L, Alnemri D, Cingolani G, Alnemri E (2017) Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/apoptotic cell death. Nat Commun 8:14128PubMedPubMedCentralCrossRefGoogle Scholar
  86. Rozina E, Kaptsova T, Sharova O, Nikolaeva M, Nesterova T (1984) Study of mumps virus invasiveness in monkeys. Acta Virol 28(2):107–113PubMedPubMedCentralGoogle Scholar
  87. Rudd P, Cattaneo R, von Messling V (2006) Canine distemper virus uses both the anterograde and hematogenous pathway for neuroinvasion. J Virol 80:9361–9370PubMedPubMedCentralCrossRefGoogle Scholar
  88. Simpson RJ, Lim JW, Moritz RL, Mathivanan S (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6:267–283PubMedCrossRefPubMedCentralGoogle Scholar
  89. Song H, Moseley P, Lowe S, Ozbun M (2010) Inducible heat shock protein 70 enhances HPV31 viral genome replication and virion production during the differentiation-dependent life cycle in human keratinocytes. Virus Res 147:113–122PubMedCrossRefPubMedCentralGoogle Scholar
  90. Steel R, Doherty J, Buzzard K, Clemons N, Hawkins C, Anderson R (2004) Hsp72 inhibits apoptosis upstream of the mitochondria and not through interactions with Apaf-1. J Biol Chem 279(49):51490–51499PubMedCrossRefPubMedCentralGoogle Scholar
  91. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G (2002) The biogenesis and functions of exosomes. Traffic 3:321–330PubMedCrossRefPubMedCentralGoogle Scholar
  92. Strong M, Blanchard E, Lin Z, Morris C, Baddoo M, Taylor C, Ware M, Flemington E (2016) A comprehensive next generation sequencing-based virome assessment in brain tissue suggests no major virus-tumor association. Acta Neuropathol Commun 4(1):71PubMedPubMedCentralCrossRefGoogle Scholar
  93. Taguwa S, Maringer K, Li X, Bernal-Rubio D, Rauch J, Gestwicki J, Andino R, Fernandez-Sesma A, Frydman J (2015) Defining hsp70 subnetworks in Dengue virus replication reveals key vulnerability in flavivirus infection. Cell 163(5):1108–1123PubMedPubMedCentralCrossRefGoogle Scholar
  94. Tanguy Le G, Boehmer P (2002) Activation of the herpes simplex virus type-1 origin binding protein (UL9) by heat shock proteins. J Biol Chem 277:5660–5666CrossRefGoogle Scholar
  95. Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2:569–579PubMedCrossRefPubMedCentralGoogle Scholar
  96. Tischer S, Basila M, Maecker-Kolhoff B, Immenschuh S, Oelke M, Blasczyk R, Eiz-Vesper B (2012) Heat shock protein 70/peptide complexes: potent mediators for the generation of antiviral T cells particularly with regard to low precursor frequencies. J Transl Med 9:175CrossRefGoogle Scholar
  97. Toshchakov V, Jones B, Perera P, Thomas K, Cody M, Zhang S, Williams B, Major J, Hamilton T, Fenton M, Vogel S (2002) TLR4, but not TLR2, mediates IFN-beta-induced STAT1alpha/beta-dependent gene expression in macrophages. Nat Immunol 3:392–398PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tytell M, Brown W, Moody D, Challa V (1998) Immunohistochemical assessment of constitutive and inducible heat-shock protein 70 and ubiquitin in human cerebellum and caudate nucleus. Mol Chem Neuropathol 35:97–117PubMedCrossRefPubMedCentralGoogle Scholar
  99. Vabulas R, Ahmad-Nejad P, Ghose S, Kirschning C, Issels R, Wagner H (2002) HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277:15107–15112PubMedCrossRefPubMedCentralGoogle Scholar
  100. Vasconcelos D, Cai X, Oglesbee M (1998a) Constitutive overexpression of the major inducible 70 kDa heat shock protein mediates large plaque formation by measles virus. J Gen Virol 79:2239–2908PubMedCrossRefPubMedCentralGoogle Scholar
  101. Vasconcelos D, Norrby E, Oglesbee M (1998b) The cellular stress response increases measles virus-induced cytopathic effect. J Gen Virol 79:1769–1773PubMedCrossRefPubMedCentralGoogle Scholar
  102. von Rüden E-L, Wolf F, Keck M, Gualtieri F, Nowakowska M, Oglesbee M, Potschka H (2018) Genetic modulation of HSPA1A accelerates kindling progression and exerts pro-convulsant effects. Neuroscience 386:108–120CrossRefGoogle Scholar
  103. Weidinger G, Czub S, Neumeister C, Harriott P, ter Meulen V, Niewiesk S (2000) Role of CD4(+) and CD8(+) T cells in the prevention of measles virus-induced encephalitis in mice. J Gen Virol 81:2707–2713PubMedCrossRefPubMedCentralGoogle Scholar
  104. Wheeler D, Chase M, Senft A, Poynter S, Wong H, Page K (2009) Extracellular Hsp70, an endogenous DAMP, is released by virally infected airway epithelial cells and activates neutrophils via Toll-like receptor (TLR)-4. Respir Res 10:31PubMedPubMedCentralCrossRefGoogle Scholar
  105. Wu YP, Chang CM, Hung CY, Tsai MC, Schuyler S, Wang R (2011) Japanese encephalitis virus co-opts the ER-stress response protein GRP78 for viral infectivity. Virol J 8:128PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ye J, Chen Z, Zhang B, Miao H, Zohaib A, Xu Q, Chen H, Cao S (2013) Heat shock protein 70 is associated with replicase complex of Japanese encephalitis virus and positively regulates viral genome replication. PLoS One 8:e75188PubMedPubMedCentralCrossRefGoogle Scholar
  107. Yuyama K, Sun H, Mitsutake S, Igarashi Y (2012) Sphingolipid-modulated exosome secretion promotes clearance of amyloid beta by microglia. J Biol Chem 287:10977–10989PubMedPubMedCentralCrossRefGoogle Scholar
  108. Zhang X, Glendening C, Linke H, Parks C, Brooks C, Udem S, Oglesbee M (2002a) Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J Virol 76(17):8737–8746PubMedPubMedCentralCrossRefGoogle Scholar
  109. Zhang Y, Huang L, Zhang J, Moskophidis D, Mivechi N (2002b) Targeted disruption of hsf1 leads to lack of thermotolerance and defines tissue-specific regulation for stress-inducible Hsp molecular chaperones. J Cell Biochem 86(2):376–393PubMedCrossRefPubMedCentralGoogle Scholar
  110. Zhang X, Bourhis J, Longhi S, Carsillo T, Buccellato M, Morin B, Canard B, Oglesbee M (2005) Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337:162–174PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Michael Oglesbee
    • 1
    Email author
  • Mi Young Kim
    • 2
  • Yaoling Shu
    • 3
  • Sonia Longhi
    • 4
  1. 1.Department of Veterinary BiosciencesThe Ohio State UniversityColumbusUSA
  2. 2.Pharmaceutical Safety Evaluation DivisionMinistry of Food and Drug SafetyCheongjuRepublic of Korea
  3. 3.Department of Neuroscience, Center for Brain and Spinal Cord RepairThe Ohio State UniversityColumbusUSA
  4. 4.CNRS, Architecture et Fonction des Macromolécules Biologiques (AFMB), UMRAix-Marseille UnivMarseilleFrance

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