Systemic infections and inflammation affect chronic neurodegeneration (original) (raw)

• Combrinck, M. I., Perry, V. H. & Cunningham, C. Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease. Neuroscience 112, 7–11 (2002).
  Article CAS PubMed Google Scholar
• Cunningham, C., Wilcockson, D. C., Campion, S., Lunnon, K. & Perry, V. H. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J. Neurosci. 25, 9275–9284 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Dantzer, R. Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 500, 399–411 (2004).
  Article CAS PubMed Google Scholar
• Tracey, K. J. The inflammatory reflex. Nature 420, 853–859 (2002).
  Article CAS PubMed Google Scholar
• Laflamme, N. & Rivest, S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor κBα within specific cellular populations of the rat brain. J. Neurochem. 73, 309–321 (1999).
  Article CAS PubMed Google Scholar
• Chakravarty, S. & Herkenham, M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J. Neurosci. 25, 1788–1796 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Ek, M. et al. Inflammatory response: pathway across the blood–brain barrier. Nature 410, 430–431 (2001).
  Article CAS PubMed Google Scholar
• Perry, V. H. & Gordon, S. Macrophages and microglia in the nervous system. Trends Neurosci. 11, 273–277 (1988).
  Article CAS PubMed Google Scholar
• Nimmerjahn, A., Kirchhoff, F. & Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314–1318 (2005).
  Article CAS PubMed Google Scholar
• Hoek, R. M. et al. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290, 1768–1771 (2000).
  Article CAS PubMed Google Scholar
• Mott, R. T. et al. Neuronal expression of CD22: novel mechanism for inhibiting microglial proinflammatory cytokine production. Glia 46, 369–379 (2004).
  Article PubMed Google Scholar
• Daws, M. R. et al. Pattern recognition by TREM-2: binding of anionic ligands. J. Immunol. 171, 594–599 (2003).
  Article CAS PubMed Google Scholar
• Schmid, C. D. et al. Heterogeneous expression of the triggering receptor expressed on myeloid cells-2 on adult murine microglia. J. Neurochem. 83, 1309–1320 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Kreutzberg, G. W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312–318 (1996).
  Article CAS PubMed Google Scholar
• Raivich, G. et al. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res. Brain Res. Rev. 30, 77–105 (1999).
  Article CAS PubMed Google Scholar
• Gordon, S. Alternative activation of macrophages. Nature Rev. Immunol. 3, 23–35 (2003).
  Article CAS Google Scholar
• Stout, R. D. et al. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175, 342–349 (2005).
  Article CAS PubMed Google Scholar
• Etminan, M., Gill, S. & Samii, A. Effect of non-steroidal anti-inflammatory drugs on risk of Alzheimer's disease: systematic review and meta-analysis of observational studies. BMJ 327, 128 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, H. et al. Nonsteroidal antiinflammatory drug use and the risk for Parkinson's disease. Ann. Neurol. 58, 963–967 (2005).
  Article CAS PubMed Google Scholar
• Akiyama, H. et al. Inflammation and Alzheimer's disease. Neurobiol. Aging 21, 383–421 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• McGeer, P. L., Itagaki, S., Tago, H. & McGeer, E. G. Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci. Lett. 79, 195–200 (1987).
  Article CAS PubMed Google Scholar
• Simard, A. R., Soulet, D., Gowing, G., Julien, J. P. & Rivest, S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49, 489–502 (2006).
  Article CAS PubMed Google Scholar
• D'Andrea, M. R., Cole, G. M. & Ard, M. D. The microglial phagocytic role with specific plaque types in the Alzheimer disease brain. Neurobiol. Aging 25, 675–683 (2004).
  Article CAS PubMed Google Scholar
• Combs, C. K., Karlo, J. C., Kao, S. C. & Landreth, G. E. β-Amyloid stimulation of microglia and monocytes results in TNFα-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J. Neurosci. 21, 1179–1188 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Brown, D. R., Schmidt, B. & Kretzschmar, H. A. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345–347 (1996).
  Article CAS PubMed Google Scholar
• Bamberger, M. E., Harris, M. E., McDonald, D. R., Husemann, J. & Landreth, G. E. A cell surface receptor complex for fibrillar β-amyloid mediates microglial activation. J. Neurosci. 23, 2665–2674 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Koenigsknecht, J. & Landreth, G. Microglial phagocytosis of fibrillar β-amyloid through a β1 integrin-dependent mechanism. J. Neurosci. 24, 9838–9846 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Ajmone-Cat, M. A., Nicolini, A. & Minghetti, L. Prolonged exposure of microglia to lipopolysaccharide modifies the intracellular signaling pathways and selectively promotes prostaglandin E2 synthesis. J. Neurochem. 87, 1193–1203 (2003).
  Article CAS PubMed Google Scholar
• Griffin, W. S. & Mrak, R. E. Interleukin-1 in the genesis and progression of and risk for development of neuronal degeneration in Alzheimer's disease. J. Leukoc. Biol. 72, 233–238 (2002).
  CAS PubMed Google Scholar
• Lim, G. P. et al. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J. Neurosci. 20, 5709–5714 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Lim, G. P. et al. Ibuprofen effects on Alzheimer pathology and open field activity in APPsw transgenic mice. Neurobiol. Aging 22, 983–991 (2001).
  Article CAS PubMed Google Scholar
• Quinn, J. et al. Inflammation and cerebral amyloidosis are disconnected in an animal model of Alzheimer's disease. J. Neuroimmunol. 137, 32–41 (2003).
  Article CAS PubMed Google Scholar
• Sly, L. M. et al. Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer's disease. Brain Res. Bull. 56, 581–588 (2001).
  Article CAS PubMed Google Scholar
• Wyss-Coray, T. et al. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc. Natl Acad. Sci. USA 99, 10837–10842 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hensley, K. et al. Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J. Neurochem. 82, 365–374 (2002).
  Article CAS PubMed Google Scholar
• Hensley, K. et al. Message and protein-level elevation of tumor necrosis factor α (TNFα) and TNFα-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol. Dis. 14, 74–80 (2003).
  Article CAS PubMed Google Scholar
• Nguyen, M. D., Julien, J. P. & Rivest, S. Induction of proinflammatory molecules in mice with amyotrophic lateral sclerosis: no requirement for proapoptotic interleukin-1β in neurodegeneration. Ann. Neurol. 50, 630–639 (2001).
  Article CAS PubMed Google Scholar
• Depino, A. M. et al. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur. J. Neurosci. 18, 2731–2742 (2003).
  Article PubMed Google Scholar
• Sriram, K. et al. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. FASEB J. 16, 1474–1476 (2002).
  Article CAS PubMed Google Scholar
• Rousselet, E. et al. Role of TNF-α receptors in mice intoxicated with the parkinsonian toxin MPTP. Exp. Neurol. 177, 183–192 (2002).
  Article CAS PubMed Google Scholar
• Leng, A., Mura, A., Feldon, J. & Ferger, B. Tumor necrosis factor-α receptor ablation in a chronic MPTP mouse model of Parkinson's disease. Neurosci. Lett. 375, 107–111 (2005).
  Article CAS PubMed Google Scholar
• Brown, A. R. et al. Inducible cytokine gene expression in the brain in the ME7/CV mouse model of scrapie is highly restricted, is at a strikingly low level relative to the degree of gliosis and occurs only late in disease. J. Gen. Virol. 84, 2605–2611 (2003).
  Article CAS PubMed Google Scholar
• Cunningham, C., Wilcockson, D. C., Boche, D. & Perry, V. H. Comparison of inflammatory and acute-phase responses in the brain and peripheral organs of the ME7 model of prion disease. J. Virol. 79, 5174–5184 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Cunningham, C., Boche, D. & Perry, V. H. Transforming growth factor β1, the dominant cytokine in murine prion disease: influence on inflammatory cytokine synthesis and alteration of vascular extracellular matrix. Neuropathol. Appl. Neurobiol. 28, 107–119 (2002).
  Article CAS PubMed Google Scholar
• Felton, L. M. et al. MCP-1 and murine prion disease: Separation of early behavioural dysfunction from overt clinical disease. Neurobiol. Dis. 20, 283–295 (2005).
  Article CAS PubMed Google Scholar
• Mabbott, N. A. et al. Tumor necrosis factor α-deficient, but not interleukin-6-deficient, mice resist peripheral infection with scrapie. J. Virol. 74, 3338–3344 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Schultz, J. et al. Role of interleukin-1 in prion disease-associated astrocyte activation. Am. J. Pathol. 165, 671–678 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Bogdan, C., Paik, J., Vodovotz, Y. & Nathan, C. Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-β and interleukin-10. J. Biol. Chem. 267, 23301–23308 (1992).
  CAS PubMed Google Scholar
• McDonald, P. P., Fadok, V. A., Bratton, D. & Henson, P. M. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells. J. Immunol. 163, 6164–6172 (1999).
  CAS PubMed Google Scholar
• Schook, L. B., Albrecht, H., Gallay, P. & Jongeneel, C. V. Cytokine regulation of TNF-α mRNA and protein production by unprimed macrophages from C57Bl/6 and NZW mice. J. Leukoc. Biol. 56, 514–520 (1994).
  Article CAS PubMed Google Scholar
• Chantry, D., Turner, M., Abney, E. & Feldmann, M. Modulation of cytokine production by transforming growth factor-β. J. Immunol. 142, 4295–4300 (1989).
  CAS PubMed Google Scholar
• Ye, S. M. & Johnson, R. W. An age-related decline in interleukin-10 may contribute to the increased expression of interleukin-6 in brain of aged mice. Neuroimmunomodulation 9, 183–192 (2001).
  Article CAS PubMed Google Scholar
• De Simone, R., Ajmone-Cat, M. A., Carnevale, D. & Minghetti, L. Activation of α7 nicotinic acetylcholine receptor by nicotine selectively up-regulates cyclooxygenase-2 and prostaglandin E2 in rat microglial cultures. J. Neuroinflammation 2, 4 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Cunningham, C. et al. Synaptic changes characterize early behavioural changes in the ME7 model of murine prion disease. Eur. J. Neurosci. 17, 2147–2155 (2003).
  Article CAS PubMed Google Scholar
• Boche, D., Cunningham, C., Docagne, F., Scott, H. & Perry, V. H. TGFβ1 regulates the inflammatory response during chronic neurodegeneration. Neurobiol. Dis. 22, 638–650 (2006).
  Article CAS PubMed Google Scholar
• Thackray, A. M., McKenzie, A. N., Klein, M. A., Lauder, A. & Bujdoso, R. Accelerated prion disease in the absence of interleukin-10. J. Virol. 78, 13697–13707 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• DiCarlo, G., Wilcock, D., Henderson, D., Gordon, M. & Morgan, D. Intrahippocampal LPS injections reduce Aβ load in APP+PS1 transgenic mice. Neurobiol. Aging 22, 1007–1012 (2001).
  Article CAS PubMed Google Scholar
• Herber, D. L. et al. Time-dependent reduction in Aβ levels after intracranial LPS administration in APP transgenic mice. Exp. Neurol. 190, 245–253 (2004).
  Article CAS PubMed Google Scholar
• Wilcock, D. M. et al. Microglial activation facilitates Aβ plaque removal following intracranial anti-Aβ antibody administration. Neurobiol. Dis. 15, 11–20 (2004).
  Article CAS PubMed Google Scholar
• Bard, F. et al. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nature Med. 6, 916–919 (2000).
  Article CAS PubMed Google Scholar
• Schenk, D. et al. Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400, 173–177 (1999).
  Article CAS PubMed Google Scholar
• Perry, V. H., Newman, T. A. & Cunningham, C. The impact of systemic infection on the progression of neurodegenerative disease. Nature Rev. Neurosci. 4, 103–112 (2003).
  Article CAS Google Scholar
• Godbout, J. P. et al. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19, 1329–1331 (2005).
  Article CAS PubMed Google Scholar
• Perry, V. H., Matyszak, M. K. & Fearn, S. Altered antigen expression of microglia in the aged rodent CNS. Glia 7, 60–67 (1993).
  Article CAS PubMed Google Scholar
• Godbout, J. P. & Johnson, R. W. Interleukin-6 in the aging brain. J. Neuroimmunol. 147, 141–144 (2004).
  Article CAS PubMed Google Scholar
• Kyrkanides, S., O'Banion, M. K., Whiteley, P. E., Daeschner, J. C. & Olschowka, J. A. Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury. J. Neuroimmunol. 119, 269–277 (2001).
  Article CAS PubMed Google Scholar
• Barrientos, R. M. et al. Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol. Aging 27, 723–732 (2006).
  Article PubMed Google Scholar
• Lee, J., Chan, S. L. & Mattson, M. P. Adverse effect of a presenilin-1 mutation in microglia results in enhanced nitric oxide and inflammatory cytokine responses to immune challenge in the brain. Neuromolecular Med. 2, 29–45 (2002).
  Article CAS PubMed Google Scholar
• Kitazawa, M., Oddo, S., Yamasaki, T. R., Green, K. N. & LaFerla, F. M. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J. Neurosci. 25, 8843–8853 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Nguyen, M. D., D'Aigle, T., Gowing, G., Julien, J. P. & Rivest, S. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 24, 1340–1349 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• McCusker, J., Cole, M., Dendukuri, N., Belzile, E. & Primeau, F. Delirium in older medical inpatients and subsequent cognitive and functional status: a prospective study. Can. Med. Assoc. J. 165, 575–583 (2001).
  CAS Google Scholar
• Rahkonen, T., Luukkainen-Markkula, R., Paanila, S., Sivenius, J. & Sulkava, R. Delirium episode as a sign of undetected dementia among community dwelling elderly subjects: a 2 year follow up study. J. Neurol. Neurosurg. Psychiatry 69, 519–521 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Fick, D. M., Agostini, J. V. & Inouye, S. K. Delirium superimposed on dementia: a systematic review. J. Am. Geriatr. Soc. 50, 1723–1732 (2002).
  Article PubMed Google Scholar
• 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. 19, 91–94 (2005).
  Article PubMed Google Scholar
• Engelhart, M. J. et al. Inflammatory proteins in plasma and the risk of dementia: The Rotterdam Study. Arch. Neurol. 61, 668–672 (2004).
  Article PubMed Google Scholar
• Tilvis, R. S. et al. Predictors of cognitive decline and mortality of aged people over a 10-year period. J. Gerontol. A 59, 268–274 (2004).
  Article Google Scholar
• Ott, A. et al. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 53, 1937–1942 (1999).
  Article CAS PubMed Google Scholar
• Andersen, K., Lolk, A., Kragh-Sorensen, P., Petersen, N. E. & Green, A. Depression and the risk of Alzheimer disease. Epidemiology 16, 233–238 (2005).
  Article PubMed Google Scholar
• Fleminger, S., Oliver, D. L., Lovestone, S., Rabe-Hesketh, S. & Giora, A. Head injury as a risk factor for Alzheimer's disease: the evidence 10 years on; a partial replication. J. Neurol. Neurosurg. Psychiatry 74, 857–862 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Craig, D., Mirakhur, A., Hart, D. J., McIlroy, S. P. & Passmore, A. P. A cross-sectional study of neuropsychiatric symptoms in 435 patients with Alzheimer's disease. Am. J. Geriatr. Psychiatry 13, 460–468 (2005).
  Article PubMed Google Scholar
• Starkstein, S. E., Jorge, R., Mizrahi, R. & Robinson, R. G. A prospective longitudinal study of apathy in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 77, 8–11 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Hope, T., Keene, J., Fairburn, C. G., Jacoby, R. & McShane, R. Natural history of behavioural changes and psychiatric symptoms in Alzheimer's disease. A longitudinal study. Br. J. Psychiatry 174, 39–44 (1999).
  Article CAS PubMed Google Scholar
• Yip, A. G., Brayne, C. & Matthews, F. E. Risk factors for incident dementia in England and Wales: The Medical Research Council Cognitive Function and Ageing Study. A population-based nested case-control study. Age Ageing 35, 154–160 (2006).
  Article PubMed Google Scholar
• Robert, P. H. et al. Apathy in patients with mild cognitive impairment and the risk of developing dementia of Alzheimer's disease. A one-year follow-up study. Clin. Neurol. Neurosurg. 108, 733–736 (2006).
  Article PubMed Google Scholar
• American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) 4th edn (American Psychiatric Association, Washington DC, 1994).
• Clark, C. M. et al. Variability in annual Mini-Mental State Examination score in patients with probable Alzheimer disease: a clinical perspective of data from the Consortium to Establish a Registry for Alzheimer's Disease. Arch. Neurol. 56, 857–862 (1999).
  Article CAS PubMed Google Scholar
• Holmes, C. & Lovestone, S. Long-term cognitive and functional decline in late onset Alzheimer's disease: therapeutic implications. Age Ageing 32, 200–204 (2003).
  Article PubMed Google Scholar
• Holmes, C. et al. Systemic infection, interleukin 1β, and cognitive decline in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 74, 788–789. (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Hart, B. L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12, 123–137 (1988).
  Article CAS PubMed Google Scholar
• Blond, D., Campbell, S. J., Butchart, A. G., Perry, V. H. & Anthony, D. C. Differential induction of interleukin-1β and tumour necrosis factor-α may account for specific patterns of leukocyte recruitment in the brain. Brain Res. 958, 89–99 (2002).
  Article CAS PubMed Google Scholar