Neuroinflammation resulting from covert brain invasion by common viruses - A potential role in local and global neurodegeneration

Medical Hypotheses

Volumn 75, Issue 2, 2010, Pages 204-213

  Majde, Jeannine A ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 2 INHIBITOR; CYTOKINE; FISH OIL; LIVE VACCINE; MINOCYCLINE; OMEGA 3 FATTY ACID; PARACETAMOL; VIRUS VACCINE;

ALZHEIMER DISEASE; ARTICLE; BRAIN INFECTION; CLINICAL RESEARCH; DEGENERATIVE DISEASE; ENCEPHALITIS; GLIA CELL; HUMAN; HYPOTHALAMUS; INFLUENZA; MULTIPLE SCLEROSIS; NERVE CELL NETWORK; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NEUROTROPISM; NONHUMAN; NOSE CAVITY; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY NERVE; PATHOGENESIS; PNEUMONIA; RESPIRATORY TRACT DISEASE; RESPIRATORY VIRUS; VIRUS INFECTION; AGED; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN CORTEX; INTRANASAL DRUG ADMINISTRATION; MOUSE; NERVE CELL; RISK; VIROLOGY; VIRUS;

ADMINISTRATION, INTRANASAL; AGED; ANIMALS; BRAIN; CEREBRAL CORTEX; CYTOKINES; HUMANS; INFLUENZA, HUMAN; MICE; MODELS, BIOLOGICAL; NERVE DEGENERATION; NEURODEGENERATIVE DISEASES; NEURONS; OLFACTORY BULB; OLFACTORY NERVE; RISK; VIRUSES;

MUS;

EID: 77954311350     PISSN: 03069877     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mehy.2010.02.023     Document Type: Article

References (157)

1. Mattson M.P. Infectious agents and age-related neurodegenerative disorders. Ageing Res Rev 2004, 3(1):105-120.
2. Hirtz D., Thurman D.J., Gwinn-Hardy K., Mohamed M., Chaudhuri A.R., Zalutsky R. How common are the " common" neurologic disorders?. Neurology 2007, 68(5):326-337.
3. Kristensson K. Avian influenza and the brain - comments on the occasion of resurrection of the Spanish flu virus. Brain Res Bull 2006, 68:406-413.
4. Vahlenkamp T.W., Enbergs H.K., Muller H. Experimental and natural Borna disease virus infections: presence of viral RNA in cells of the peripheral blood. Vet Microbiol 2000, 76(3):229-244.
5. Yolken R.H. Viruses and schizophrenia: a focus on herpes simplex virus. Herpes 2007, 11(Suppl. 2):83A-88A.
6. Sierra-Honigmann A.M., Carbone K.M., Yolken R.H. Polymerase chain reaction (PCR) search for viral nucleic acid sequences in schizophrenia. Br J Psychiatry 1995, 166(1):55-60.
7. McCall S., Henry J.M., Reid A.H., Taubenberger J.K. Influenza RNA not detected in archival brain tissues from acute encephalitis lethargica cases or in postencephalitic Parkinson cases. J Neuropathol Exp Neurol 2001, 60:696-704.
8. Atkins G.J., McQuaid S., Morris-Downes M.M., Galbraith S.E., Amor S., Cosby S.L., et al. Transient virus infection and multiple sclerosis. Rev Med Virol 2000, 10(5):291-303.
9. Strous R.D., Shoenfeld Y. To smell the immune system: olfaction, autoimmunity and brain involvement. Autoimm Rev 2006, 6(1):54-60.
10. Doty R.L. Studies of human olfaction from the University of Pennsylvania Smell and Taste Center. Chem Senses 1997, 22(5):565-586.
11. Johnson R.T., Mims C.A. Pathogenesis of viral infections of the nervous system. N Engl J Med 1968, 278(1):23-30.
12. Mohammed A.H., Norrby E., Kristensson K. Viruses and behavioural changes: a review of clinical and experimental findings. Rev Neurosci 1993, 4(3):267-286.
13. Doty R.L. The olfactory vector hypothesis of neurodegenerative disease: is it viable?. Ann Neurol 2008, 63(1):7-15.
14. Majde J.A., Bohnet S.G., Ellis G.A., Churchill L., Leyva-Grado V., Wu M., et al. Detection of mouse-adapted human influenza virus in the olfactory bulb of mice within hours after intranasal infection. J Neurovirol 2007, 13(5):399-409.
15. Cagnin A., Kassiou M., Meikle S.R., Banati R.B. In vivo evidence for microglial activation in neurodegenerative dementia. Acta Neurol Scand 2006, 114(s185):107-114.
16. Ghafouri M., Amini S., Khalili K., Sawaya B.E. HIV-1 associated dementia: symptoms and causes. Retrovirol 2006, 3(May 19):28-39.
17. Lassmann H., Bruck W., Lucchinetti C.F. The immunopathology of multiple sclerosis: an overview. Brain Pathol 2007, 17(2):210-218.
18. Thanvi B., Lo N., Robinson T. Essential tremor - the most common movement disorder in older people. Age Ageing 2006, 35(4):344-349.
19. Terry R.D. Alzheimer's disease and the aging brain. J Geriatr Psychiatry Neurol 2006, 19(3):125-128.
20. Frank-Cannon T, Alto L, McAlpine F, Tansey M. Does neuroinflammation fan the flame in neurodegenerative diseases? Available from: ; 2009. http://www.molecularneurodegeneration.com/content/4/1/47.
21. Brown R.C., Lockwood A.H., Sonawane B.R. Neurodegenerative diseases: an overview of environmental risk factors. Environ Health Perspect 2005, 113(9):1250-1256.
22. Mangano E.N., Hayley S. Inflammatory priming of the substantia nigra influences the impact of later paraquat exposure: neuroimmune sensitization of neurodegeneration. Neurobiol Aging 2009, 30:1361-1378.
23. Perry V.H., Cunningham C., Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 2007, 7(2):161-167.
24. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 2005, 76(2):77-98.
25. Prediger R.D., Rial D., Medeiros R., Figueiredo C.P., Doty R.L., Takahashi R.N. Risk is in the air: an intranasal MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) rat model of Parkinson's disease. Ann NY Acad Sci 2009, 1170:629-636.
26. Chen J.K., Johnston K.M., Petrides M., Ptito A. Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Arch Gen Psychiatry 2008, 65(1):81-89.
27. Sayer N.A., Chiros C.E., Sigford B., Scott S., Clothier B., Pickett T., et al. Characteristics and rehabilitation outcomes among patients with blast and other injuries sustained during the global war on terror. Arch Phys Med Rehab 2008, 89(1):163-170.
28. Martin L.J., Al-Abdulla N.A., Brambrink A.M., Kirsch J.R., Sieber F.E., Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 1998, 46(4):281-309.
29. Gentile D.A., Doyle W.J., Zeevi A., Piltcher O., Skoner D.P. Cytokine gene polymorphisms moderate responses to respiratory syncytial virus in adults. Hum Immunol 2003, 64:93-98.
30. Waters R.J., Nicoll J.A. Genetic influences on outcome following acute neurological insults. Curr Opinion Crit Care 2005, 11(2):105-110.
31. Fortunato G., Calcagno G., Bresciamorra V., Salvatore E., Filla A., Capone S., et al. Multiple sclerosis and hepatitis C virus infection are associated with single nucleotide polymorphisms in interferon pathway genes. J Interferon Cytokine Res 2008, 28(3):141-152.
32. Giunta B, Fernandez F, Nikolic WV, Obregon D, Rrapo E, Town T, et al. Inflammaging as a prodrome to Alzheimer's disease. Available from: ; 2008. http://www.jneuroinflammation.com/content/5/1/51.
33. Loseva E., Yuan T.F., Karnup S. Neurogliogenesis in the mature olfactory system: a possible protective role against infection and toxic dust. Brain Res Rev 2009, 59(2):374-387.
34. Beutler B., Eidenschenk C., Crozat K., Imler J.L., Takeuchi O., Hoffmann J.A., et al. Genetic analysis of resistance to viral infection. Nat Rev Immunol 2007, 7(10):753-766.
35. Shipley, MT, Ennis M, Puche AC. Olfactory system. In: Paxinos G, editor. The rat nervous system. 3rd ed. San Diego; 2004. p. 923-64.
36. Leyva-Grado V., Churchill L., Wu M., Williams T.J., Majde J.A., Taishi P., et al. Influenza virus- and cytokine-immunoreactive cells in the murine olfactory and central autonomic nervous systems before and after illness onset. J Neuroimmunol 2009, 211:73-83.
37. Mori I., Goshima F., Ito H., Koide N., Yoshida T., Yokochi T., et al. The vomeronasal chemosensory system as a route of neuroinvasion by herpes simplex virus. Virology 2005, 334(1):51-58.
38. Mori I., Nishiyama Y., Yokochi T., Kimura Y. Olfactory transmission of neurotropic viruses. J Neurovirol 2005, 11(2):129-137.
39. Schlesinger R.W., Husak P.J., Bradshaw G.L., Panayotov P.P. Mechanisms involved in natural and experimental neuropathogenicity of influenza viruses: evidence and speculation. Adv Virus Res 1998, 50:289-379.
40. Li Y., Field P.M., Raisman G. Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 2005, 52(3):245-251.
41. Elder A., Gelein R., Silva V., Feikert T., Opanashuk L., Carter J., et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect 2006, 114(8):1172-1178.
42. Illum L. Transport of drugs from the nasal cavity to the central nervous system. Eur J Pharmaceut Sci 2000, 11(1):1-18.
43. Fiske B.K., Brunjes P.C. Microglial activation in the developing rat olfactory bulb. Neuroscience 2000, 96(4):807-815.
44. Biber K., Neumann H., Inoue K., Boddeke H.W.G.M. Neuronal 'on' and 'off' signals control microglia. Trends Neurosci 2007, 30(11):596-602.
45. Rosenberg G.A. Matrix metalloproteinases and neuroinflammation in multiple sclerosis. Neuroscientist 2002, 8(6):586-595.
46. Deng Y., Thompson B.M., Gao X., Hall E.D. Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp Neurol 2007, 205(1):154-165.
47. Simi A., Tsakiri N., Wang P., Rothwell N.J. Interleukin-1 and inflammatory neurodegeneration. Biochem Soc Transact 2007, 035(5):1122-1126.
48. Sriram U., Biswas C., Behrens E.M., Dinnall J.A., Shivers D.K., Monestier M., et al. IL-4 suppresses dendritic cell response to type I interferons. J Immunol 2007, 179(10):6446-6455.
49. Cacquevel M., Lebeurrier N., Cheenne D., Vivien D. Cytokines in neuroinflammation and Alzheimers disease. Curr Drug Targets 2004, 5:529-534.
50. Rothwell N.J., Relton J.K. Involvement of cytokines in acute neurodegeneration in the CNS. Neurosci Biobehav Rev 1993, 17(2):217-227.
51. Chao C.C., Hu S.X., Ehrlich L., Peterson P.K. Interleukin-1 and tumor necrosis factor-α synergistically mediate neurotoxicity: Involvement of nitric oxide and of N-methyl-d-aspartate receptors. Brain Behav Immun 1995, 9(4):355-365.
52. Brabers N.A., Nottet H.S. Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur J Clin Invest 2006, 36(7):447-458.
53. Esiri M.M. The interplay between inflammation and neurodegeneration in CNS disease. J Neuroimmunol 2007, 184(1-2):4-16.
54. Bulloch K., Miller M.M., Gal-Toth J., Milner T.A., Gottfried A.B., Waters E.M., et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult and injured mouse brain. J Comp Neurol 2008, 508:687-710.
55. Traynor T.R., Majde J.A., Bohnet S.G., Krueger J.M. Interferon type I receptor-deficient mice have altered disease symptoms in response to influenza virus. Brain Behav Immun 2007, 21:311-322.
56. Amadori M. The role of IFN-alpha as homeostatic agent in the inflammatory response: a balance between danger and response?. J Interferon Cytokine Res 2007, 27(3):181-190.
57. Taylor J.L., Grossberg S.E. The effects of interferon-α on the production and action of other cytokines. Semin Oncol 1998, 25(Suppl. 1):23-29.
58. Li X., Hanson C., Cmarik J.L., Ruscetti S. Neurodegeneration induced by PVC-211 murine leukemia virus is associated with increased levels of vascular endothelial growth factor and macrophage inflammatory protein 1α and is inhibited by blocking activation of microglia. J Virol 2009, 83(10):4912-4922.
59. Ludwiczek O., Kaser A., Koch R.O., Vogel W., Cruikshank W.W., Tilg H. Activation of caspase-3 by interferon alpha causes interleukin-16 secretion but fails to modulate activation induced cell death. Eur Cytokine Netw 2001, 12(3):478-486.
60. Akwa Y., Hassett D.E., Eloranta M.L., Sandberg K., Masliah E., Powell H., et al. Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration. J Immunol 1998, 161(9):5016-5026.
61. Enevold C., Oturai A.B., Sorensen P.S., Ryder L.P., Koch-Henriksen N., Bendtzen K. Multiple sclerosis and polymorphisms of innate pattern recognition receptors TLR1-10, NOD1-2, DDX58, and IFIH1. J Neuroimmunol 2009, 212:125-131.
62. Scott K., Manunta M., Germain C., Smith P., Jones M., Mitchell P., et al. Qualitatively distinct patterns of cytokines are released by human dendritic cells in response to different pathogens. Immunology 2005, 116(2):245-254.
63. Mori I., Goshima F., Koshizuka T., Koide N., Sugiyama T., Yoshida T., et al. Differential activation of the c-Jun N-terminal kinase/stress-activated protein kinase and p38 mitogen-activated protein kinase signal transduction pathways in the mouse brain upon infection with neurovirulent influenza A virus. J Gen Virol 2003, 84(Pt 9):2401-2408.
64. Boggian I., Buzzacaro E., Calistri A., Calvi P., Cavaggioni A., Mucignat-Caretta C., et al. Asymptomatic herpes simplex type 1 virus infection of the mouse brain. J Neurovirol 2000, 6(4):303-313.
65. Perlman S., Sun N., Barnett E.M. Spread of MHV-JHM from nasal cavity to white matter of spinal cord. Transneuronal movement and involvement of astrocytes. Adv Exp Med Biol 1995, 380:73-78.
66. Rudd P.A., Cattaneo R., von Messling V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J Virol 2006, 80(19):9361-9370.
67. Yoon H.A., Eo S.K., Aleyas A.G., Cha S.Y., Lee J.H., Chae J.S., et al. Investigation of pseudorabies virus latency in nervous tissues of seropositive pigs exposed to field strain. J Vet Med Sci 2006, 68(2):143-148.
68. Takahashi M., Yamada T., Nakajima S., Nakajima K., Yamamoto T., Okada H. The substantia nigra is a major target for neurovirulent influenza A virus. J Exp Med 1995, 181(6):2161-2169.
69. Bradshaw G.L., Schlesinger R.W., Schwartz C.D. Effects of cell differentiation on replication of A/WS/33, WSN, and A/PR/8/34 influenza viruses in mouse brain cell cultures: biological and immunological characterization of products. J Virol 1989, 63:1704-1714.
70. Bright R.A., Cho D.S., Rowe T., Katz J.M. Mechanisms of pathogenicity of influenza A (H5N1) viruses in mice. Avian Dis 2003, 47(3 Suppl.):1131-1134.
71. Bohnet S.G., Sawatzki N., Majde J.A., Churchill L., Krueger J.M. Persistent brain infection of PR8 influenza at 48 and 96 hours post-infection. Sleep 2009, 32(Abstract Suppl.):A402.
72. Chao C.C., Hu S., Peterson P.K. Glia: the not so innocent bystanders. J Neurovirol 1996, 2(4):234-239.
73. Hall E.D., Sullivan P.G., Gibson T.R., Pavel K.M., Thompson B.M., Scheff S.W. Spatial and temporal characteristics of neurodegeneration after controlled cortical impact in mice. more than a focal brain injury. J Neurotrauma 2005, 22(2):252-265.
74. Hawkes C. Olfaction in neurodegenerative disorder. Adv Otorhinolaryngol 2006, 63:133-151.
75. Welge-Lussen A., Wolfensberger M. Olfactory disorders following upper respiratory tract infections. Adv Otorhinolaryngol 2006, 63:125-132.
76. Sugiura M., Aiba T., Mori J., Nakai Y. An epidemiological study of postviral olfactory disorder. Acta Oto-laryngol 1998, 538(6 Suppl. 538):191-196.
77. Henkin R.I., Larson A.L., Powell R.D. Hypogeusia, dysgeusia, hyposmia, and dysosmia following influenza-like infection. Ann Oto Rhino Laryngol 1975, 84(5 Pt 1):672-682.
78. Suzuki M., Saito K., Min W.P., Vladau C., Toida K., Itoh H., et al. Identification of viruses in patients with postviral olfactory dysfunction. Laryngoscope 2007, 117(2):272-277.
79. Harris R., Davidson T.M., Murphy C., Gilbert P.E., Chen M. Clinical evaluation and symptoms of chemosensory impairment: one thousand consecutive cases from the nasal dysfunction Clinic in San Diego. Am J Rhinol 2006, 20(1):101-108.
80. Schiffman S.S. Critical illness and changes in sensory perception. Proc Nutr Soc 2007, 66(03):331-345.
81. Levy L.M., Henkin R.I., Lin C.S., Finley A. Rapid imaging of olfaction by functional MRI (fMRI): identification of presence and type of hyposmia. J Comput Assisted Tomography 1999, 23(5):767-775.
82. Mizuguchi M., Yamanouchi H., Ichiyama T., Shiomi M. Acute encephalopathy associated with influenza and other viral infections. Acta Neurol Scand 2007, 115(s186):45-56.
83. Yao D., Kuwajima M., Chen Y., Shiota M., Okumura Y., Yamada H., et al. Impaired long-chain fatty acid metabolism in mitochondria causes brain vascular invasion by a non-neurotropic epidemic influenza A virus in the newborn/suckling period: implications for influenza-associated encephalopathy. Mol Cell Biochem 2007, 299(1):85-92.
84. Antonucci R., Fanos V. Acute encephalopathy associated with respiratory syncytial virus infections in childhood. A literature review. Minerva Pediatr 2005, 57(3):137-142.
85. Hayase Y., Tobita K. Influenza virus and neurological diseases. Psychiatry Clin Neurosci 1997, 51(4):181-184.
86. Yokota S. Influenza-associated encephalopathy-pathophysiology and disease mechanisms. Nip Rinsho 2003, 61(11):1953-1958.
87. Centers for Disease Control and Prevention (CDC) Neurologic complications associated with novel influenza A (H1N1) virus infection in children - Dallas, Texas, May 2009. MMWR: Morbidity and Mortality Weekly Report 2009, 58(28):773-778.
88. Sasseville V.G., Lackner A.A. Neuropathogenesis of simian immunodeficiency virus infection in macaque monkeys. J Neurovirol 1997, 3(1):1-9.
89. Khalili K., White M.K. Human demyelinating disease and the polyomavirus JCV. Mult Scler 2006, 12(2):133-142.
90. Ravits J. Sporadic amyotrophic lateral sclerosis: a hypothesis of persistent (non-cytolytic) enteroviral infection. Amyotroph Lateral Scler Other Motor Neuron Disord 2005, 6(2):77-87.
91. Frank O., Giehl M., Zheng C., Hehlmann R., Leib-Mosch C., Seifarth W. Human endogenous retrovirus expression profiles in samples from brains of patients with schizophrenia and bipolar disorders. J Virol 2005, 79(17):10890-10901.
92. Hobbs J.A. Detection of adeno-associated virus 2 and parvovirus B19 in the human dorsolateral prefrontal cortex. J Neurovirol 2006, 12(3):190-199.
93. Gordon L., McQuaid S., Cosby S.L. Detection of herpes simplex virus (types 1 and 2) and human herpesvirus 6 DNA in human brain tissue by polymerase chain reaction. Clin Diagn Virol 1996, 6(1):33-40.
94. Yolken R.H., Torrey E.F. Viruses, schizophrenia, and bipolar disorder. Clin Microbiol Rev 1995, 8:131-145.
95. Haga S., Yoshimura M., Motoi Y., Arima K., Aizawa T., Ikuta K., et al. Detection of Borna disease virus genome in normal human brain tissue. Brain Res 1997, 770(1-2):307-309.
96. Niebuhr D.W., Millikan A.M., Cowan D.N., Yolken R., Li Y., Weber N.S. Selected infectious agents and risk of schizophrenia among US military personnel. Am J Psychiatry 2008, 165(1):99-106.
97. Leweke F.M., Gerth C., Koethe D., Klosterklotter J., Ruslanova I., Krivogorsky B., et al. Antibodies to infectious agents in individuals with recent onset schizophrenia. Eur Arch Psychiatry Clin Neurosci 2004, 254(1):4-8.
98. Steiner I., Nisipianu P., Wirguin I. Infection and the etiology and pathogenesis of multiple sclerosis. Curr Neurol Neurosci Rep 2001, 1(3):271-276.
99. Takahashi M., Yamada T. Viral etiology for Parkinson's disease - a possible role of influenza A virus infection. Jpn J Infect Dis 1999, 52(3):89-98.
100. Ottolini M.G., Burnett M.W. History of US military contributions to the study of respiratory infections. Mil Med 2005, 170(4 Suppl.):66-70.
101. Dale R.C., Church A.J., Surtees R.A.H., Lees A.J., Adcock J.E., Harding B., et al. Encephalitis lethargica syndrome: 20 new cases and evidence of basal ganglia autoimmunity. Brain 2004, 127(Pt1):21-33.
102. Casals J., Elizan T.S., Yahr M.D. Postencephalitic parkinsonism - a review. J Neural Transm 1998, 105(6-7):645-676.
103. Hawkes C.H., Del T.K., Braak H. Parkinson's disease: the dual hit theory revisited. Ann NY Acad Sci 2009, 1170:615-622.
104. Franco J., Prediger R.D.S., Pandolfo P., Takahashi R.N., Farina M., Dafre A.L. Antioxidant responses and lipid peroxidation following intranasal 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) administration in rats: increased susceptibility of olfactory bulb. Life Sci 2007, 80(20):1906-1914.
105. Koponen H., Rantakallio P., Veijola J., Jones P., Jokelainen J., Isohanni M. Childhood central nervous system infections and risk for schizophrenia. Eur Arch Psychiatry Clin Neurosci 2004, 254(1):9-13.
106. Brown A.S., Begg M.D., Gravenstein S., Schaefer C.A., Wyatt R.J., Bresnahan M., et al. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 2004, 61(8):774-780.
107. Bernstein H.G., Steiner J., Bogerts B. Glial cells in schizophrenia: pathophysiological significance and possible consequences for therapy. Expert Rev Neurotherap 2009, 9(7):1059-1071.
108. Westergaard T., Mortensen P.B., Pedersen C.B., Wohlfahrt J., Melbye M. Exposure to prenatal and childhood infections and the risk of schizophrenia: suggestions from a study of sibship characteristics and influenza prevalence. Arch Gen Psychiatry 1999, 56(11):993-998.
109. Jensen-Fangel S., Mohey R., Johnsen S.P., Andersen P.L., Sorensen H.T., Ostergaard L. Gender differences in hospitalization rates for respiratory tract infections in Danish youth. Scand J Infect Dis 2004, 36(1):31-36.
110. Gilmore J.H., Jarskog L.F., Vadlamudi S. Maternal poly I:C exposure during pregnancy regulates TNFα, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. J Neuroimmunol 2005, 159(1-2):106-112.
111. Ovanesov MV, Moldovan K, Smith K, Vogel MW, Pletnikov MV. Persistent Borna disease virus (BDV) infection activates microglia prior to a detectable loss of granule cells in the hippocampus. Available from: ; 2008. http://www.jneuroinflammation.com/content/5/1/16.
112. Zachary J.F., Baszler T.V., French R.A., Kelley K.W. Mouse Moloney leukemia virus infects microglia but not neurons even though it induces motor neuron disease. Mol Psychiatry 1997, 2(2):104-106.
113. Perry V.H., Newman T.A., Cunningham C. The impact of systemic infection on the progression of neurodegenerative disease. Nat Rev Neurosci 2003, 4(2):103-112.
114. Mori K., Kaneko Y.S., Nakashima A., Nagatsu I., Takahashi H., Ota A. Peripheral lipopolysaccharide induces apoptosis in the murine olfactory bulb. Brain Res 2005, 1039(1-2):116-129.
115. Dunn N., Mullee M., Perry V.H., Holmes C. Association between dementia and infectious disease: evidence from a case-control study. Alzheimer Dis Assoc Disord 2005, 19(2):91-94.
116. Teeling J.L., Felton L.M., Deacon R.M.J., Cunningham C., Rawlins J.N.P., Perry V.H. Sub-pyrogenic systemic inflammation impacts on brain and behavior, independent of cytokines. Brain Behav Immun 2007, 21(6):836-850.
117. Holmes C., Cunningham C., Zotova E., Woolford J., Dean C., Kerr S., et al. Systemic inflammation and disease progression in Alzheimer disease. Neurology 2009, 73(10):768-774.
118. Martyn C.N. Infection in childhood and neurological diseases in adult life. Br Med Bull 1997, 53(1):24-39.
119. Sharma A., Valadi N., Miller A.H., Pearce B.D. Neonatal viral infection decreases neuronal progenitors and impairs adult neurogenesis in the hippocampus. Neurobiol Dis 2002, 11(2):246-256.
120. Chen J., Buchanan J.B., Sparkman N.L., Godbout J.P., Freund G.G., Johnson R.W. Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 2008, 22(3):301-311.
121. Sieve A.N., Steelman A.J., Young C.R., Storts R., Welsh T.H., Welsh C.J., et al. Chronic restraint stress during early Theiler's virus infection exacerbates the subsequent demyelinating disease in SJL mice. J Neuroimmunol 2004, 155(1-2):103-118.
122. Olson J.K., Girvin A.M., Miller S.D. Direct activation of innate and antigen-presenting functions of microglia following infection with Theiler's virus. J Virol 2001, 75(20):9780-9789.
123. Guida J.D., Fejer G., Pirofski L.A., Brosnan C.F., Horwitz M.S. Mouse adenovirus type 1 causes a fatal hemorrhagic encephalomyelitis in adult C57BL/6 but not BALB/c mice. J Virol 1995, 69(12):7674-7681.
124. Karupiah G. Type 1 and type 2 cytokines in antiviral defense. Vet Immunol Immunopathol 1998, 63(1-2):105-109.
125. Christian A.Y., Barna M., Bi Z., Reiss C.S. Host immune response to vesicular stomatitis virus infection of the central nervous system in C57BL/6 mice. Viral Immunol 1996, 9(3):195-205.
126. Barna M., Komatsu T., Bi Z., Reiss C.S. Sex differences in susceptibility to viral infection of the central nervous system. J Neuroimmunol 1996, 67(1):31-39.
127. Rogers E., Wagner A.K. Gender, sex steroids, and neuroprotection following traumatic brain injury. J Head Trauma Rehab 2006, 21(3):279-281.
128. Marchetti B., Serra P.A., L'Episcopo F., Tirolo C., Caniglia S., Testa N., et al. Hormones are key actors in gene x environment interactions programming the vulnerability to Parkinson's disease: glia as a common final pathway. Ann NY Acad Sci 2005, 1057(Dec):296-318.
129. Webber K.M., Casadesus G., Perry G., Atwood C.S., Bowen R., Smith M.A. Gender differences in Alzheimer disease: the role of luteinizing hormone in disease pathogenesis. Alzheimer Dis Assoc Disord 2005, 19(2):95-99.
130. Schwendimann RN, Alekseeva N. Gender issues in multiple sclerosis. In: Alireza M, editor. International review of neurobiology - the neurobiology of multiple sclerosis, vol. 79. San Diego; 2007. p. 377-92.
131. Koskiniemi M., Rantalaiho T., Piiparinen H., Von Bonsdorff C.H., Farkkila M., Jarvinen A., et al. Infections of the central nervous system of suspected viral origin: a collaborative study from Finland. J Neurovirol 2001, 7(5):400-408.
132. Lemiale F., Kong W.p., Akyurek L.M., Ling X., Huang Y., Chakrabarti B.K., et al. Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J Virol 2003, 77(18):10078-10087.
133. Kritas S.K., Nauwynck H.J., Pensaert M.B., Kyriakis S.C. Effect of the concentration of maternal antibodies on the neural invasion of Aujeszky's disease virus in neonatal pigs. Vet Microbiol 1997, 55(1-4):29-36.
134. Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002, 8(3):448-460.
135. Stern R.A., Silva S.G., Chaisson N., Evans D.L. Influence of cognitive reserve on neuropsychological functioning in asymptomatic human immunodeficiency virus-1 infection. Arch Neurol 1996, 53(2):148-153.
136. Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord 2006, 20(3 Suppl. 2):S69-S74.
137. Gibbs E.L., Gibbs F.A., Grossman H. Electroencephalographic evidence of encephalitis in children with supposedly " uncomplicated" childhood diseases. Trans Am Neurol Assoc 1956, 159-160. 81st Meeting.
138. Grossman H.J., Gibbs E.L., Spies H.W. Electroencephalographic studies on children having measles with no clinical evidence of involvement of the central nervous system. Pediatrics 1956, 18(4):556-560.
139. Csernansky J.G. Neurodegeneration in schizophrenia: evidence from in vivo neuroimaging studies. Sci World J 2007, 7(2):135-143.
140. Apostolova L.G., Thompson P.M. Brain mapping as a tool to study neurodegeneration. Neurotherapeutics 2007, 4(3):387-400.
141. Majde J.A. Microbial cell-wall contaminants in peptides: a potential source of physiological artifacts. Peptides 1993, 14:629-632.
142. Ma Y.P., Ma M.M., Ge S., Guo R.B., Zhang H.J., Frey W.H., et al. Intranasally delivered TGF-β1 enters brain and regulates gene expressions of its receptors in rats. Brain Res Bull 2007, 74(4):271-277.
143. Minghetti L., Greco A., Potenza R.L., Pezzola A., Blum D., Bantubungi K., et al. Effects of the adenosine A2A receptor antagonist SCH 58621 on cyclooxygenase-2 expression, glial activation, and brain-derived neurotrophic factor availability in a rat model of striatal neurodegeneration. J Neuropathol Exp Neurol 2007, 66(5):363-371.
144. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., et al. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 2002, 22(5):1763-1771.
145. Farooqui A.A., Ong W.Y., Horrocks L.A., Chen P., Farooqui T. Comparison of biochemical effects of statins and fish oil in brain: the battle of the titans. Brain Res Rev 2007, 56(2):443-471.
146. Wolozin B., Wang S.W., Li N.-C., Lee A., Lee T.A., Kazis L.E. Simvastatin is associated with a reduced incidence of dementia and Parkinson's disease. BMC Med 2007, 5(July):20-31.
147. Kakar P., Watson T., Lip G.Y. New approaches to therapy with omega-3 fatty acids. Curr Atheroscler Rep 2008, 10(1):79-87.
148. Moore M.E., Piazza A., McCartney Y., Lynch M.A. Evidence that vitamin D3 reverses age-related inflammatory changes in the rat hippocampus. Biochem Soc Transact 2005, 33(Pt 4):573-577.
149. McCann J.C., Ames B.N. Is there convincing biological or behavioral evidence linking vitamin D deficiency to brain dysfunction?. FASEB J 2008, 22(4):982-1001.
150. Laflamme N., Lacroix S., Rivest S. An essential role of interleukin-1beta in mediating NF-kappaB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia. J Neurosci 1999, 19(24):10923-10930.
151. Garcia-Bueno B., Madrigal J.L., Lizasoain I., Moro M.A., Lorenzo P., Leza J.C. Peroxisome proliferator-activated receptor gamma activation decreases neuroinflammation in brain after stress in rats. Biol Psychiatry 2005, 57(8):885-894.
152. Strauss K.I. Antiinflammatory and neuroprotective actions of COX2 inhibitors in the injured brain. Brain Behav Immun 2008, 22(3):285-298.
153. Tripathy D, Grammas P. Acetaminophen inhibits neuronal inflammation and protects neurons from oxidative stress. Available from: ; 2009. http://www.jneuroinflammation.com/content/6/1/10.
154. Skaper S.D. The brain as a target for inflammatory processes and neuroprotective strategies. Ann NY Acad Sci 2007, 1122(1):23-34.
155. Vink R., Nimmo A.J. Multifunctional drugs for head injury. Neurotherapeutics 2009, 6(1):28-42.
156. Dantzer R., Kelley K.W. Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 2007, 21(2):153-160.
157. Leyva-Grado V., Churchill L., Harding J., Krueger J.M. The olfactory nerve has a role in the body temperature and brain cytokine responses to influenza virus. Brain Behav Imm 2010, 24:281-288.