CoChat
Sign Up
Cited by 89Neuroinflammation and Neurodegeneration MechanismsMosquito-borne diseases and controlParkinson's Disease Mechanisms and Treatments

Infection with mosquito-borne alphavirus induces selective loss of dopaminergic neurons, neuroinflammation and widespread protein aggregation

Open access
Bantle, Collin M., Phillips, Aaron T., Smeyne, Richard J., Rocha, Savannah M., Olson, Ken E., Tjalkens, Ronald B.·2019·npj Parkinson's Disease
DOI 10.1038/s41531-019-0090-8PMC PMC6744428
Open this paper in CoChat — free account

Abstract

Neuroinvasive infections with mosquito-borne alphaviruses such as Western equine encephalitis virus (WEEV) can cause post-encephalitic parkinsonism. To understand the mechanisms underlying these neurological effects, we examined the capacity of WEEV to induce progressive neurodegeneration in outbred CD-1 mice following non-lethal encephalitic infection. Animals were experientally infected with recombinant WEEV expressing firefly luciferase or dsRed (RFP) reporters and the extent of viral replication was controlled using passive immunotherapy. WEEV spread along the neuronal axis from the olfactory bulb to the entorhinal cortex, hippocampus and basal midbrain by 4 days post infection (DPI). Infection caused activation of microglia and astrocytes, selective loss of dopaminergic neurons in the substantia nigra pars compacta (SNpc) and neurobehavioral abnormalities. After 8 weeks, surviving mice displayed continued loss of dopamine neurons in the SNpc, lingering glial cell activation and gene expression profiles consistent with a neurodegenerative phenotype. Strikingly, prominent proteinase K-resistant protein aggregates were present in the the entorhinal cortex, hippocampus and basal midbrain that stained positively for phospho-serine129 α-synuclein (SNCA). These results indicate that WEEV may cause lasting neurological deficits through a severe neuroinflammatory response promoting both neuronal injury and protein aggregation in surviving individuals.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41531-019-0090-8

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Viral infections may play a role in developing and progressing neurodegenerative disorders, particularly Alzheimer's disease.

    “suggesting a potential role in developing and progressing neurodegenerative disorders, particularly AD (Bantle et al., 2019; Piekut et al., 2022; Ronca et al., 2017).”

    From Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model (2024) · cites this paper as Bantle et al., 2019

    The Discussion says viral infection is a possible risk factor for neurodegenerative diseases, explicitly including Alzheimer’s disease. The Introduction also describes viral infection as a potential contributor to multiple neurodegenerative diseases. The paper does not specifically establish a role in Alzheimer’s disease progression or give AD particular emphasis; its experiments focus on Parkinson’s-like pathology in mice. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • Viral infections such as Herpes simplex encephalitis, Epstein-Barr virus, Eastern Equine Encephalitis virus, Western Equine Encephalitis virus, and Venezuelan Equine Encephalitis Virus correlate with negative neurological consequences even after the acute phase.

    “Several studies have shown that viral infections, such as Herpes simplex encephalitis, Epstein-Barr virus, Eastern Equine Encephalitis virus (EEEV), Western Equine Encephalitis virus (WEEV), and Venezuelan Equine Encephalitis Virus (VEEV), correlate with negative neurological consequences even after the acute phase”

    From Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model (2024) · cites this paper as Bantle et al., 2019

    The Introduction reports neurological symptoms persisting long after acute WEEV infection, and the Discussion describes deficits in mice eight weeks after infection. The Discussion also mentions neurological injury associated with Epstein–Barr virus, but does not establish that it persists after the acute phase. The retrieved passages do not establish post-acute neurological consequences for herpes simplex encephalitis, EEEV, or VEEV; EEEV and VEEV appear only in references to other work. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • WEEV infection in a rodent model produces phospho-serine129 alpha-synuclein positive, proteinase K-resistant protein aggregates, indicating neurological sequelae and neuronal injury consistent with a Parkinson's neurodegenerative phenotype.

    “Interestingly, phospho-serine129 α-synuclein positive, proteinase K-resistant protein aggregates are also present, indicating neurological sequelae and neuronal injury consistent with Parkinson's neurodegenerative phenotype (Bantle et al., 2019).”

    From Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model (2024) · cites this paper as Bantle et al., 2019

  • WEEV infection in a rodent model leads to glial cell activation and acute and chronic loss of dopaminergic neurons in the substantia nigra pars compacta.

    “For example, WEEV infection in a rodent model leads to glial cell activation and acute and chronic loss of dopaminergic neurons in the substantia nigra pars compacta (Bantle et al., 2019).”

    From Arbovirus infection increases the risk for the development of neurodegenerative disease pathology in the murine model (2024) · cites this paper as Bantle et al., 2019

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 84 · Cited by 89

Research works printed but not linked: 81

  1. [1]De Chiara G Infectious agents and neurodegeneration Mol. Neurobiol. 2012 46 614 638 10.1007/s12035-012-8320-7 22899188 PMC3496540 · DOI
  2. [2]Jang H Boltz DA Webster RG Smeyne RJ Viral parkinsonism Biochim Biophys. Acta 2009 7 714 721 10.1016/j.bbadis.2008.08.001 PMC4642437 18760350 · DOI
  3. [3]Limongi D Baldelli S Redox imbalance and viral infections in neurodegenerative diseases Oxid. Med. Cell. Longev. 2016 2016 6547248 10.1155/2016/6547248 27110325 PMC4826696 · DOI
  4. [4]Mattson MP Infectious agents and age-related neurodegenerative disorders Ageing Res Rev. 2004 3 105 120 10.1016/j.arr.2003.08.005 15163105 PMC7172323 · DOI
  5. [5]Eimer WA Alzheimer’s disease-associated beta-amyloid is rapidly seeded by herpesviridae to protect against brain infection Neuron 2018 99 56 63 10.1016/j.neuron.2018.06.030 30001512 PMC6075814 · DOI · Paper page
  6. [6]Dourmashkin RR What caused the 1918-30 epidemic of encephalitis lethargica? J. R. Soc. Med. 1997 90 515 520 10.1177/014107689709000916 9370993 PMC1296535 · DOI
  7. [7]Reid AH McCall S Henry JM Taubenberger JK Experimenting on the past: the enigma of von Economo’s encephalitis lethargica J. Neuropathol. Exp. Neurol. 2001 60 663 670 10.1093/jnen/60.7.663 11444794 · DOI
  8. [8]Henry J Smeyne RJ Jang H Miller B Okun MS Parkinsonism and neurological manifestations of influenza throughout the 20th and 21st centuries Park. Relat. Disord. 2010 16 566 571 10.1016/j.parkreldis.2010.06.012 PMC4684089 20650672 · DOI
  9. [9]Phillips AT Entry sites of Venezuelan and western equine encephalitis viruses in the mouse central nervous system following peripheral infection J. Virol. 2016 90 5785 5796 10.1128/JVI.03219-15 27053560 PMC4886771 · DOI
  10. [11]Levine B Griffin DE Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis J. Virol. 1992 66 6429 6435 1383564 PMC240135
  11. [12]Zhou Y Frey TK Yang JJ Viral calciomics: interplays between Ca(2+) and virus Cell Calcium 2009 46 1 17 10.1016/j.ceca.2009.05.005 19535138 PMC3449087 · DOI
  12. [13]Schultz DR Barthal JS Garrett C Western equine encephalitis with rapid onset of parkinsonism Neurology 1977 27 1095 1096 10.1212/WNL.27.11.1095 563006 · DOI
  13. [14]Mogi M Kondo T Mizuno Y Nagatsu T p53 protein, interferon-gamma, and NF-kappaB levels are elevated in the parkinsonian brain Neurosci. Lett. 2007 414 94 p97 10.1016/j.neulet.2006.12.003 17196747 · DOI
  14. [15]Reale M Peripheral cytokines profile in Parkinson’s disease Brain Behav. Immun. 2009 23 55 63 10.1016/j.bbi.2008.07.003 18678243 · DOI · Paper page
  15. [16]Dobbs RJ Association of circulating TNF-alpha and IL-6 with ageing and parkinsonism Acta Neurol. Scand. 1999 100 34 41 10.1111/j.1600-0404.1999.tb00721.x 10416510 · DOI
  16. [17]Silva da Costa L Pereira da Silva AP Da Poian AT El-Bacha T Mitochondrial bioenergetic alterations in mouse neuroblastoma cells infected with Sindbis virus: implications to viral replication and neuronal death PLoS ONE 2012 7 2 10.1371/journal.pone.0033871 PMC3317446 22485151 · DOI
  17. [18]Braak H Staging of brain pathology related to sporadic Parkinson’s disease Neurobiol. Aging 2003 24 197 211 10.1016/S0197-4580(02)00065-9 12498954 · DOI · Paper page
  18. [19]Braak H Rub U Gai WP Del Tredici K Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen J. Neural Transm. (Vienna) 2003 110 517 536 10.1007/s00702-002-0808-2 12721813 · DOI · Paper page
  19. [20]Phillips AT Bioluminescent imaging and histopathologic characterization of WEEV neuroinvasion in outbred CD-1 mice PLoS ONE 2013 8 2 PMC3534643 23301074
  20. [21]Phillips AT Liposome-antigen-nucleic acid complexes protect mice from lethal challenge with western and eastern equine encephalitis viruses J. Virol. 2014 88 1771 1780 10.1128/JVI.02297-13 24257615 PMC3911585 · DOI
  21. [22]Rico AB Venezuelan and western equine encephalitis virus E1 liposome antigen nucleic acid complexes protect mice from lethal challenge with multiple alphaviruses Virology 2016 499 30 39 10.1016/j.virol.2016.08.023 27632563 PMC5884135 · DOI
  22. [23]Wang XH Quantitative assessment of gait and neurochemical correlation in a classical murine model of Parkinson’s disease BMC Neurosci. 2012 13 142 10.1186/1471-2202-13-142 23151254 PMC3507899 · DOI
  23. [24]Fricke IB 6-hydroxydopamine-induced Parkinson’s disease-like degeneration generates acute microgliosis and astrogliosis in the nigrostriatal system but no bioluminescence imaging-detectable alteration in adult neurogenesis Eur. J. Neurosci. 2016 43 1352 1365 10.1111/ejn.13232 26950181 · DOI
  24. [25]Barcia C Glial-mediated inflammation underlying parkinsonism Scientifica 2013 2013 357805 10.1155/2013/357805 24278772 PMC3820356 · DOI
  25. [26]Rothhammer V Microglial control of astrocytes in response to microbial metabolites Nature 2018 557 724 728 10.1038/s41586-018-0119-x 29769726 PMC6422159 · DOI · Paper page
  26. [27]Beatman EL Alpha-synuclein expression restricts RNA viral infections in the brain J. Virol. 2015 90 2767 2782 10.1128/JVI.02949-15 26719256 PMC4810656 · DOI
  27. [28]Jang H Boltz DA Webster RG Smeyne RJ Viral parkinsonism Biochim Biophys. Acta 2009 1792 714 721 10.1016/j.bbadis.2008.08.001 18760350 PMC4642437 · DOI
  28. [29]Jang H Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration Proc. Natl Acad. Sci. USA 2009 106 14063 14068 10.1073/pnas.0900096106 19667183 PMC2729020 · DOI
  29. [30]Caggiu E Inflammation, infectious triggers, and Parkinson’s disease Front Neurol. 2019 10 122 10.3389/fneur.2019.00122 30837941 PMC6389614 · DOI
  30. [31]Anderson JP Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease J. Biol. Chem. 2006 281 29739 29752 10.1074/jbc.M600933200 16847063 · DOI
  31. [32]Yang Y Japanese encephalitis virus infection induces changes of mRNA profile of mouse spleen and brain Virol. J. 2011 8 80 10.1186/1743-422X-8-80 21345237 PMC3056812 · DOI
  32. [33]Oliveira TG Di Paolo G Phospholipase D in brain function and Alzheimer’s disease Biochim Biophys. Acta 2010 1801 799 805 10.1016/j.bbalip.2010.04.004 20399893 PMC3328196 · DOI
  33. [34]Ihle NT Abraham RT The Pten-Parkin Axis: at the nexus of cancer and neurodegeneration Mol. Cell 2017 65 959 960 10.1016/j.molcel.2017.02.030 28306509 · DOI
  34. [35]He S Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke Autophagy 2012 8 1621 1627 10.4161/auto.21561 22874556 PMC3494591 · DOI
  35. [36]Lewy FH Die Entstehung der Einschlußkörper und ihre Bedeutung für die systematische Einordnung der sogenannten Viruskrankheiten Dtsch. Z. f.ür. Nervenheilkd. 1932 124 93 100 10.1007/BF01652906 · DOI
  36. [37]Cook SH Griffin DE Luciferase Imaging of neurotropic viral infection in intact animals J. Virol. 2003 77 5333 5338 10.1128/JVI.77.9.5333-5338.2003 12692235 PMC153972 · DOI
  37. [38]Du L Richter JD Activity-dependent polyadenylation in neurons RNA 2005 11 1340 1347 10.1261/rna.2870505 16043499 PMC1370817 · DOI
  38. [40]Richter JD CPEB: a life in translation Trends Biochem. Sci. 2007 32 279 285 10.1016/j.tibs.2007.04.004 17481902 · DOI
  39. [41]Darnell, J. C. & Richter, J. D. Cytoplasmic RNA-binding proteins and the control of complex brain function. Cold Spring Harb. Perspect. Biol. 4, 1–17 (2012). PMC3405866 22723494
  40. [42]Huang YS Carson JH Barbarese E Richter JD Facilitation of dendritic mRNA transport by CPEB Genes Dev. 2003 17 638 653 10.1101/gad.1053003 12629046 PMC196011 · DOI
  41. [43]Attems J Jellinger KA The dorsal motor nucleus of the vagus is not an obligatory trigger site of Parkinson’s disease Neuropathol. Appl. Neurobiol. 2008 34 466 467 10.1111/j.1365-2990.2008.00937.x 18282157 · DOI
  42. [44]Kalaitzakis ME Graeber MB Gentleman SM Pearce RK Controversies over the staging of alpha-synuclein pathology in Parkinson’s disease Acta Neuropathol. 2008 116 125 128 10.1007/s00401-008-0381-3 18446352 · DOI
  43. [45]Elizan TS Casals J Astrogliosis in von Economo’s and postencephalitic Parkinson’s diseases supports probable viral etiology J. Neurol. Sci. 1991 105 131 134 10.1016/0022-510X(91)90135-T 1757788 · DOI
  44. [47]Wyrsch P Blenn C Bader J Althaus FR Cell death and autophagy under oxidative stress: roles of poly(ADP-Ribose) polymerases and Ca2+ Mol. Cell Biol. 2012 32 3541 3553 10.1128/MCB.00437-12 22751932 PMC3422003 · DOI
  45. [48]Gullberg RC Jordan Steel J Moon SL Soltani E Geiss BJ Oxidative stress influences positive strand RNA virus genome synthesis and capping Virology 2015 475 219 229 10.1016/j.virol.2014.10.037 25514423 PMC4332586 · DOI
  46. [49]Wang Louisa M-C Dragich Joanna M Kudo Takashi Odom Irene H Welsh David K O'Dell Thomas J Colwell Christopher S Expression of the Circadian Clock GenePeriod2in the Hippocampus: Possible Implications for Synaptic Plasticity and Learned Behaviour ASN Neuro 2009 1 3 AN20090020 10.1042/AN20090020 PMC2695588 19570032 · DOI
  47. [50]Wang LM Suthana NA Chaudhury D Weaver DR Colwell CS Melatonin inhibits hippocampal long-term potentiation Eur. J. Neurosci. 2005 22 2231 2237 10.1111/j.1460-9568.2005.04408.x 16262661 PMC2581482 · DOI
  48. [51]Wong TP Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment Proc. Natl Acad. Sci. USA 2007 104 11471 11476 10.1073/pnas.0702308104 17592137 PMC2040922 · DOI
  49. [52]Wilde GJ Pringle AK Wright P Iannotti F Differential vulnerability of the CA1 and CA3 subfields of the hippocampus to superoxide and hydroxyl radicals in vitro J. Neurochem. 1997 69 883 886 10.1046/j.1471-4159.1997.69020883.x 9231752 · DOI
  50. [53]Cree BC Bernardini GL Hays AP Lowe G A fatal case of coxsackievirus B4 meningoencephalitis Arch. Neurol. 2003 60 107 112 10.1001/archneur.60.1.107 12533096 · DOI
  51. [54]Roselli F Reversible Parkinsonian syndrome associated with anti-neuronal antibodies in acute EBV encephalitis: a case report Park. Relat. Disord. 2006 12 257 260 10.1016/j.parkreldis.2005.11.004 16459123 · DOI
  52. [55]Dimova PS Bojinova V Georgiev D Milanov I Acute reversible parkinsonism in Epstein-Barr virus-related encephalitis lethargica-like illness Mov. Disord. 2006 21 564 566 10.1002/mds.20742 16250020 · DOI
  53. [56]Hsieh JC Lue KH Lee YL Parkinson-like syndrome as the major presenting symptom of Epstein-Barr virus encephalitis Arch. Dis. Child 2002 87 358 10.1136/adc.87.4.358 12244024 PMC1763051 · DOI
  54. [57]Murgod UA Muthane UB Ravi V Radhesh S Desai A Persistent movement disorders following Japanese encephalitis Neurology 2001 57 2313 2315 10.1212/WNL.57.12.2313 11756619 · DOI
  55. [58]Hersh BP Rajendran PR Battinelli D Parkinsonism as the presenting manifestation of HIV infection: improvement on HAART Neurology 2001 56 278 279 10.1212/WNL.56.2.278 11160977 · DOI
  56. [59]Mattos JP Rosso AL Correa RB Novis SA Movement disorders in 28 HIV-infected patients Arq. Neuropsiquiatr. 2002 60 525 530 10.1590/S0004-282X2002000400002 12244384 · DOI
  57. [60]Berger JR Arendt G HIV dementia: the role of the basal ganglia and dopaminergic systems J. Psychopharmacol. 2000 14 214 221 10.1177/026988110001400304 11106299 · DOI
  58. [61]Ogata A Tashiro K Nukuzuma S Nagashima K Hall WW A rat model of Parkinson’s disease induced by Japanese encephalitis virus J. Neurovirol 1997 3 141 147 10.3109/13550289709015803 9111176 · DOI
  59. [62]Stolzenberg E A role for neuronal alpha-synuclein in gastrointestinal immunity J. Innate Immun. 2017 9 456 463 10.1159/000477990 28651250 PMC5865636 · DOI
  60. [63]Duffy MF Lewy body-like alpha-synuclein inclusions trigger reactive microgliosis prior to nigral degeneration J. Neuroinflamm. 2018 15 129 10.1186/s12974-018-1171-z PMC5930695 29716614 · DOI · Paper page
  61. [64]Neumann H Kotter MR Franklin RJ Debris clearance by microglia: an essential link between degeneration and regeneration Brain 2009 132 288 295 10.1093/brain/awn109 18567623 PMC2640215 · DOI · Paper page
  62. [65]Joers V Tansey MG Mulas G Carta AR Microglial phenotypes in Parkinson’s disease and animal models of the disease Prog. Neurobiol. 2017 155 57 75 10.1016/j.pneurobio.2016.04.006 27107797 PMC5073045 · DOI · Paper page
  63. [66]Sanchez-Guajardo V Barnum CJ Tansey MG Romero-Ramos M Neuroimmunological processes in Parkinson’s disease and their relation to alpha-synuclein: microglia as the referee between neuronal processes and peripheral immunity ASN Neuro. 2013 5 113 139 10.1042/AN20120066 23506036 PMC3639751 · DOI
  64. [67]Skaper SD Facci L Zusso M Giusti P An inflammation-centric view of neurological disease: beyond the neuron Front Cell Neurosci. 2018 12 72 10.3389/fncel.2018.00072 29618972 PMC5871676 · DOI
  65. [68]Brichta L Greengard P Molecular determinants of selective dopaminergic vulnerability in Parkinson’s disease: an update Front Neuroanat. 2014 8 152 10.3389/fnana.2014.00152 25565977 PMC4266033 · DOI
  66. [69]Hirsch EC Hunot S Neuroinflammation in Parkinson’s disease: a target for neuroprotection? Lancet Neurol. 2009 8 382 397 10.1016/S1474-4422(09)70062-6 19296921 · DOI · Paper page
  67. [70]Ludlow M Neurotropic virus infections as the cause of immediate and delayed neuropathology Acta Neuropathol. 2016 131 159 184 10.1007/s00401-015-1511-3 26659576 PMC4713712 · DOI
  68. [71]Sperlagh B Illes P Purinergic modulation of microglial cell activation Purinergic Signal 2007 3 117 127 10.1007/s11302-006-9043-x 18404425 PMC2096753 · DOI
  69. [72]Clarke P Death receptor-mediated apoptotic signaling is activated in the brain following infection with West Nile virus in the absence of a peripheral immune response J. Virol. 2014 88 1080 1089 10.1128/JVI.02944-13 24198425 PMC3911655 · DOI
  70. [73]Rey NL Widespread transneuronal propagation of alpha-synucleinopathy triggered in olfactory bulb mimics prodromal Parkinson’s disease J. Exp. Med. 2016 213 1759 1778 10.1084/jem.20160368 27503075 PMC4995088 · DOI
  71. [75]Bruck D Wenning GK Stefanova N Fellner L Glia and alpha-synuclein in neurodegeneration: A complex interaction Neurobiol. Dis. 2016 85 262 274 10.1016/j.nbd.2015.03.003 25766679 PMC4730552 · DOI
  72. [76]Antipova D Bandopadhyay R Expression of DJ-1 in neurodegenerative disorders Adv. Exp. Med. Biol. 2017 1037 25 43 10.1007/978-981-10-6583-5_3 29147901 · DOI
  73. [77]Lian H Astrocyte-microglia cross talk through complement activation modulates amyloid pathology in mouse models of Alzheimer’s disease J. Neurosci. 2016 36 577 589 10.1523/JNEUROSCI.2117-15.2016 26758846 PMC4710776 · DOI · Paper page
  74. [78]Logue CH Virulence variation among isolates of western equine encephalitis virus in an outbred mouse model J. Gen. Virol. 2009 90 1848 1858 10.1099/vir.0.008656-0 19403754 PMC2887574 · DOI
  75. [79]Liu C Voth DW Rodina P Shauf LR Gonzalez G A comparative study of the pathogenesis of western equine and eastern equine encephalomyelitis viral infections in mice by intracerebral and subcutaneous inoculations J. Infect. Dis. 1970 122 53 63 10.1093/infdis/122.1-2.53 4914943 · DOI
  76. [80]Chung K Structural and molecular interrogation of intact biological systems Nature 2013 497 332 337 10.1038/nature12107 23575631 PMC4092167 · DOI · Paper page
  77. [81]Hammond SL The Nurr1 ligand, 1,1-bis(3’-indolyl)-1-(p-chlorophenyl)methane, modulates glial reactivity and is neuroprotective in MPTP-induced parkinsonism J. Pharm. Exp. Ther. 2018 365 636 651 10.1124/jpet.117.246389 PMC5941193 29626009 · DOI
  78. [82]De Miranda BR Neuroprotective efficacy and pharmacokinetic behavior of novel anti-inflammatory para-phenyl substituted diindolylmethanes in a mouse model of Parkinson’s disease J. Pharm. Exp. Ther. 2013 345 125 138 10.1124/jpet.112.201558 PMC6067390 23318470 · DOI
  79. [83]Tapias V Greenamyre JT Watkins SC Automated imaging system for fast quantitation of neurons, cell morphology and neurite morphometry in vivo and in vitro Neurobiol. Dis. 2013 54 158 168 10.1016/j.nbd.2012.11.018 23220621 PMC3604080 · DOI
  80. [84]Miller JA Runkle SA Tjalkens RB Philbert MA 1,3-Dinitrobenzene-induced metabolic impairment through selective inactivation of the pyruvate dehydrogenase complex Toxicol. Sci. 2011 122 502 511 10.1093/toxsci/kfr102 21551353 PMC3155080 · DOI
  81. [85]Gingras S SCYL2 protects CA3 pyramidal neurons from excitotoxicity during functional maturation of the mouse hippocampus J. Neurosci. 2015 35 10510 10522 10.1523/JNEUROSCI.2056-14.2015 26203146 PMC4510291 · DOI

Authors
Bantle, C. M., Phillips, A. T., Smeyne, R. J., Rocha, S. M., Olson, K. E., & Tjalkens, R. B.
Affiliations
  • Colorado State University (US)
  • Thomas Jefferson University (US)
Corresponding author
Tjalkens, Ronald B.
ORCID
Venue
npj Parkinson's Disease
Publisher
Springer Science and Business Media LLC
Published
2019-09-13
Volume
5
Issue
1
Pages
20-20
ISSN
2373-8057 (ISSN-L)
DOI
10.1038/s41531-019-0090-8
PMC
PMC6744428
OpenAlex
W2972589620
Cited by
89
References
84
Citations by year
2026: 11 · 2025: 11 · 2024: 10 · 2023: 11 · 2022: 16 · 2021: 16 · 2020: 14
FWCI
5.07
Type
journal article
Language
en
Open access
Licence
Locations
  • npj Parkinson s Disease (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Colorado State University
  • National Institute of Environmental Health Sciences (R01ES030937)
Topics
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
Keywords
western equine encephalitis virus, alphavirus, postencephalitic parkinsonism, dopaminergic neuron loss, substantia nigra pars compacta, neuroinflammation, microglial activation, astrocyte activation, protein aggregation, alpha-synuclein, neurodegeneration, olfactory bulb, entorhinal cortex, hippocampus, viral neuroinvasion, neurobehavioral abnormalities

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review