Does prior sepsis alter subsequent circadian and sickness behaviour response to lipopolysaccharide treatment in mice?

Journal of Neural Transmission

Volumn 122, Issue , 2015, Pages 63-73

  Anderson, Sean T ^a   O’Callaghan, Emma K ^a   Commins, Sean ^a   Coogan, Andrew N ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Anxiety; Circadian; Depression; LPS; Neuroimmune; Sepsis

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; LIPOPOLYSACCHARIDE; PROTEIN C FOS; CYTOKINE; POLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CIRCADIAN RHYTHM; CONTROLLED STUDY; CRYOPROTECTION; DENTATE GYRUS; HIPPOCAMPUS; ILLNESS BEHAVIOR; IMMEDIATE EARLY GENE; LOCOMOTION; MALE; MICROGLIA; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SUPRACHIASMATIC NUCLEUS; TAIL SUSPENSION TEST; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHRONOBIOLOGY DISORDERS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; IMMOBILIZATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; CHRONOBIOLOGY DISORDERS; CIRCADIAN RHYTHM; CYTOKINES; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENES, IMMEDIATE-EARLY; HINDLIMB SUSPENSION; HIPPOCAMPUS; ILLNESS BEHAVIOR; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; POLYSACCHARIDES; SEPSIS; TIME FACTORS;

EID: 84938994763     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-013-1124-8     Document Type: Article

References (43)

1. Angus DC, van der Poll T (2013) Severe sepsis and septic shock. N Engl J Med 369:840–851
2. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354
3. Beynon AL, Coogan AN (2010) Diurnal, age, and immune regulation of interleukin-1β and interleukin-1 type 1 receptor in the mouse suprachiasmatic nucleus. Chronobiol Int 27:1546–1563
4. Bonow RH, Aïd S, Zhang Y, Becker KG, Bosetti F (2009) The brain expression of genes involved in inflammatory response, the ribosome, and learning and memory is altered by centrally injected lipopolysaccharide in mice. Pharmacogenomics J 9:116–126
5. Bossù P, Cutuli D, Palladino I, Caporali P, Angelucci F, Laricchiuta D, Gelfo F, De Bartolo P, Caltagirone C, Petrosini L (2012) A single intraperitoneal injection of endotoxin in rats induces long-lasting modifications in behavior and brain protein levels of TNF-α and IL-18. J Neuroinflammation 9:101
6. Calsavara AC, Rodrigues DH, Miranda AS, Costa PA, Lima CX, Vilela MC, Rachid MA, Teixeira AL (2013) Late anxiety-like behavior and neuroinflammation in mice subjected to sublethal polymicrobial sepsis. Neurotox Res 24:103–108
7. Chen J, Buchanan JB, Sparkman NL, Godbout JP, Freund GG, Johnson RW (2008) Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 22:301–311
8. Coogan AN, Wyse CA (2008) Neuroimmunology of the circadian clock. Brain Res 1232:104–112
9. Coogan AN, Schutová B, Husung S, Furczyk K, Baune BT, Kropp P, Häßler F, Thome J (2013) The circadian system in Alzheimer’s disease: disturbances, mechanisms, and opportunities. Biol Psychiatry 74:333–339
10. Cryan JF, Mombereau C, Vassout A (2005) The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 29:571–625
11. Cunningham C (2013) Microglia and neurodegeneration: the role of systemic inflammation. Glia 61:71–90
12. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH (2005) Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275–9284
13. Dantzer R (2001) Cytokine-induced sickness behavior: mechanisms and implications. Ann N Y Acad Sci 933:222–234
14. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46–56
15. Davis S, Bozon B, Laroche S (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 142:17–30
16. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549
17. Frenois F, Moreau M, O’Connor J, Lawson M, Micon C, Lestage J, Kelley KW, Dantzer R, Castanon N (2007) Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 32:516–531
18. Gavilán MP, Castaño A, Torres M, Portavella M, Caballero C, Jiménez S, García-Martínez A, Parrado J, Vitorica J, Ruano D (2009) Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J Neurochem 108:260–267
19. Griffin EW, Skelly DT, Murray CL, Cunningham C (2013) Cyclooxygenase-1-dependent prostaglandins mediate susceptibility to systemic inflammation-induced acute cognitive dysfunction. J Neurosci 33:15248–15258
20. Hauss-Wegrzyniak B, Dobrzanski P, Stoehr JD, Wenk GL (1998) Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer’s disease. Brain Res 780:294–303
21. Henry CJ, Huang Y, Wynne AM, Godbout JP (2009) Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav Immun 23:309–317
22. Hotchkiss RS, Monneret G, Payen D (2013) Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 13:260–268
23. Iwashyna TJ, Ely EW, Smith DM, Langa KM (2010) Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 304:1787–1794
24. Kondo S, Kohsaka S, Okabe S (2011) Long-term changes of spine dynamics and microglia after transient peripheral immune response triggered by LPS in vivo. Mol Brain 4:27
25. Leone MJ, Marpegan L, Duhart JM, Golombek DA (2012) Role of proinflammatory cytokines on lipopolysaccharide-induced phase shifts in locomotor activity circadian rhythm. Chronobiol Int 29:715–723
26. Marpegán L, Bekinschtein TA, Costas MA, Golombek DA (2005) Circadian responses to endotoxin treatment in mice. J Neuroimmunol 160(1–2):102–109
27. McClung CA (2013) How might circadian rhythms control mood? Let me count the ways. Biol Psychiatry 74:242–249
28. McCusker RH, Kelley KW (2013) Immune-neural connections: how the immune system’s response to infectious agents influences behaviour. J Exp Biol 216:84–98
29. Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445–462
30. Morris M, Li L (2012) Molecular mechanisms and pathological consequences of endotoxin tolerance and priming. Arch Immunol Ther Exp (Warsz) 60:13–18
31. Norden DM, Godbout JP (2013) Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol Appl Neurobiol 39:19–34
32. O’Callaghan EK, Anderson ST, Moynagh PN, Coogan AN (2012) Long-lasting effects of sepsis on circadian rhythms in the mouse. PLoS One 7:e47087
33. Paladino N, Leone MJ, Plano SA, Golombek DA (2010) Paying the circadian toll: the circadian response to LPS injection is dependent on the Toll-like receptor 4. J Neuroimmunol 225:62–67
34. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453–462
35. Rosi S, Ramirez-Amaya V, Vazdarjanova A, Worley PF, Barnes CA (2005) Wenk GL (2005) Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J Neurosci 25:723–731
36. Semmler A, Widmann CN, Okulla T, Urbach H, Kaiser M, Widman G, Mormann F, Weide J, Fliessbach K, Hoeft A, Jessen F, Putensen C, Heneka MT (2013) Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors. J Neurol Neurosurg Psychiatry 84:62–69
37. Shaw KN, Commins S, O’Mara SM (2001) Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus. Behav Brain Res 124:47–54
38. Siami S, Annane D, Sharshar T (2008) The encephalopathy in sepsis. Crit Care Clin 24:67–82
39. Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 85:367–370
40. Vilaplana J, Lavialle M (1999) A method to quantify glial fibrillary acidic protein immunoreactivity on the suprachiasmatic nucleus. J Neurosci Methods 88:181–187
41. Weberpals M, Hermes M, Hermann S, Kummer MP, Terwel D, Semmler A, Berger M, Schäfers M, Heneka MT (2009) NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J Neurosci 29:14177–14184
42. West MA, Heagy W (2002) Endotoxin tolerance: a review. Crit Care Med 30:S64–S73
43. Yirmiya R, Rosen H, Donchin O, Ovadia H (1994) Behavioral effects of lipopolysaccharide in rats: involvement of endogenous opioids. Brain Res 648:80–86