Modulatory effects of vagal stimulation on neurophysiological parameters and the cellular immune response in the rat brain during systemic inflammation

Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 136:e28 Matsuda N, Hattori Y (2007) Vascular biology in sepsis: pathophysiological and therapeutic significance of vascular dysfunction. J Smooth Muscle Res 43:117–137 Davies MG, Hagen PO (1997) Systemic inflammatory response syndrome. Br J Surg 84:920–935 Abraham E, Anzueto A, Gutierrez G, Tessler S, San Pedro G, Wunderink R, Dal Nogare A, Nasraway S, Berman S, Cooney R, Levy H, Baughman R, Rumbak M, Light RB, Poole L, Allred R, Constant J, Pennington J, Porter S (1998) Double-blind randomised controlled trial of monoclonal antibody to human tumour necrosis factor in treatment of septic shock. NORASEPT II Study Group. Lancet 351:929–933 Abraham E, Laterre PF, Garbino J, Pingleton S, Butler T, Dugernier T, Margolis B, Kudsk K, Zimmerli W, Anderson P, Reynaert M, Lew D, Lesslauer W, Passe S, Cooper P, Burdeska A, Modi M, Leighton A, Salgo M, Van der Auwera P (2001) Lenercept (p55 tumor necrosis factor receptor fusion protein) in severe sepsis and early septic shock: a randomized, double-blind, placebo-controlled, multicenter phase III trial with 1,342 patients. Crit Care Med 29:503–510 Opal SM, Fisher CJ Jr, Dhainaut JF, Vincent JL, Brase R, Lowry SF, Sadoff JC, Slotman GJ, Levy H, Balk RA, Shelly MP, Pribble JP, LaBrecque JF, Lookabaugh J, Donovan H, Dubin H, Baughman R, Norman J, DeMaria E, Matzel K, Abraham E, Seneff M (1997) Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: a phase III, randomized, double-blind, placebo-controlled, multicenter trial. The Interleukin-1 Receptor Antagonist Sepsis Investigator Group. Crit Care Med 25:1115–1124 Martelli D, McKinley MJ, McAllen RM (2014) The cholinergic anti-inflammatory pathway: a critical review. Auton Neurosci 182:65–69 Roth J, Blatteis CM (2014) Mechanisms of fever production and lysis: lessons from experimental LPS fever. Compr Physiol 4:1563–1604 Hansen MK, Taishi P, Chen Z, Krueger JM (1998) Vagotomy blocks the induction of interleukin-1beta (IL-1beta) mRNA in the brain of rats in response to systemic IL-1beta. J Neurosci 18:2247–2253 Laye S, Bluthe RM, Kent S, Combe C, Medina C, Parnet P, Kelley K, Dantzer R (1995) Subdiaphragmatic vagotomy blocks induction of IL-1 beta mRNA in mice brain in response to peripheral LPS. Am J Physiol 268:R1327–1331 Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, Wang H, Abumrad N, Eaton JW, Tracey KJ (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405:458–462 Ziaja M (2013) Septic encephalopathy. Curr Neurol Neurosci Rep 13:383 Mihaylova S, Killian A, Mayer K, Pullamsetti SS, Schermuly R, Rosengarten B (2012) Effects of anti-inflammatory vagus nerve stimulation on the cerebral microcirculation in endotoxinemic rats. J Neuroinflammation 9:183 Mihaylova S, Schweighofer H, Hackstein H, Rosengarten B (2014) Effects of anti-inflammatory vagus nerve stimulation in endotoxemic rats on blood and spleen lymphocyte subsets. Inflamm Res 63:683–690 Dirnagl U, Kaplan B, Jacewicz M, Pulsinelli W (1989) Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model. J Cereb Blood Flow Metab 9:589–596 Ances BM, Detre JA, Takahashi K, Greenberg JH (1998) Transcranial laser doppler mapping of activation flow coupling of the rat somatosensory cortex. Neurosci Lett 257:25–28 Lindauer U, Villringer A, Dirnagl U (1993) Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. Am J Physiol 264:H1223–1228 Rosengarten B, Lutz H, Hossmann KA (2003) A control system approach for evaluating somatosensory activation by laser-Doppler flowmetry in the rat cortex. J Neurosci Methods 130:75–81 Rosengarten B, Walberer M, Allendoerfer J, Mueller C, Schwarz N, Bachmann G, Gerriets T (2008) LPS-induced endotoxic shock does not cause early brain edema formation—an MRI study in rats. Inflamm Res 57:479–483 Paxinos G WC (1998) The rat brain in stereotaxic coordinates In: Editor (ed)^(eds) Book The Rat Brain in Stereotaxic Coordinates. Academic Press, City. Damm J, Luheshi GN, Gerstberger R, Roth J, Rummel C (2011) Spatiotemporal nuclear factor interleukin-6 expression in the rat brain during lipopolysaccharide-induced fever is linked to sustained hypothalamic inflammatory target gene induction. J Comp Neurol 519:480–505 Altavilla D, Guarini S, Bitto A, Mioni C, Giuliani D, Bigiani A, Squadrito G, Minutoli L, Venuti FS, Messineo F, De Meo V, Bazzani C, Squadrito F (2006) Activation of the cholinergic anti-inflammatory pathway reduces NF-kappab activation, blunts TNF-alpha production, and protects againts splanchic artery occlusion shock. Shock 25:500–506 Guarini S, Altavilla D, Cainazzo MM, Giuliani D, Bigiani A, Marini H, Squadrito G, Minutoli L, Bertolini A, Marini R, Adamo EB, Venuti FS, Squadrito F (2003) Efferent vagal fibre stimulation blunts nuclear factor-kappaB activation and protects against hypovolemic hemorrhagic shock. Circulation 107:1189–1194 Wang Q, Cheng Y, Xue FS, Yuan YJ, Xiong J, Li RP, Liao X, Liu JH (2012) Postconditioning with vagal stimulation attenuates local and systemic inflammatory responses to myocardial ischemia reperfusion injury in rats. Inflamm Res 61:1273–1282 Zhang R, Wugeti N, Sun J, Yan H, Guo Y, Zhang L, Ma M, Guo X, Jiao C, Xu W, Li T, Liu H, Ma Y (2014) Effects of vagus nerve stimulation via cholinergic anti-inflammatory pathway activation on myocardial ischemia/reperfusion injury in canine. Int J Clin Exp Med 7:2615–2623 Rummel C (2016) Inflammatory transcription factors as activation markers and functional readouts in immune-to-brain communication. Brain Behav Immun 54:1–14 Bluthe RM, Walter V, Parnet P, Laye S, Lestage J, Verrier D, Poole S, Stenning BE, Kelley KW, Dantzer R (1994) Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R Acad Sci III 317:499–503 Dantzer R, Konsman JP, Bluthe RM, Kelley KW (2000) Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent? Auton Neurosci 85:60–65 Bluthe RM, Michaud B, Kelley KW, Dantzer R (1996) Vagotomy blocks behavioural effects of interleukin-1 injected via the intraperitoneal route but not via other systemic routes. Neuroreport 7:2823–2827 Sun Y, Li Q, Gui H, Xu DP, Yang YL, Su DF, Liu X (2013) MicroRNA-124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines. Cell Res 23:1270–1283 Rosengarten B, Hecht M, Auch D, Ghofrani HA, Schermuly RT, Grimminger F, Kaps M (2007) Microcirculatory dysfunction in the brain precedes changes in evoked potentials in endotoxin-induced sepsis syndrome in rats. Cerebrovasc Dis 23:140–147 Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232–243 Lacroix A, Toussay X, Anenberg E, Lecrux C, Ferreiros N, Karagiannis A, Plaisier F, Chausson P, Jarlier F, Burgess SA, Hillman EM, Tegeder I, Murphy TH, Hamel E, Cauli B (2015) COX-2-derived prostaglandin E2 produced by pyramidal neurons contributes to neurovascular coupling in the rodent cerebral cortex. J Neurosci 35:11791–11810 Bernzweig E, Payne JB, Reinhardt RA, Dyer JK, Patil KD (1998) Nicotine and smokeless tobacco effects on gingival and peripheral blood mononuclear cells. J Clin Periodontol 25:246–252 De Simone R, Ajmone-Cat MA, Carnevale D, Minghetti L (2005) Activation of alpha7 nicotinic acetylcholine receptor by nicotine selectively up-regulates cyclooxygenase-2 and prostaglandin E2 in rat microglial cultures. J Neuroinflammation 2:4 Payne JB, Johnson GK, Reinhardt RA, Dyer JK, Maze CA, Dunning DG (1996) Nicotine effects on PGE2 and IL-1 beta release by LPS-treated human monocytes. J Periodontal Res 31:99–104 Le Maitre E, Revathikumar P, Idborg H, Raouf J, Korotkova M, Jakobsson PJ, Lampa J (2015) Impaired vagus-mediated immunosuppression in microsomal prostaglandin E synthase-1 deficient mice. Prostaglandins Other Lipid Mediat 121:155–162 Yoshikawa H, Kurokawa M, Ozaki N, Nara K, Atou K, Takada E, Kamochi H, Suzuki N (2006) Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha7. Clin Exp Immunol 146:116–123 Sugano N, Shimada K, Ito K, Murai S (1998) Nicotine inhibits the production of inflammatory mediators in U937 cells through modulation of nuclear factor-kappaB activation. Biochem Biophys Res Commun 252:25–28 Aguilar-Valles A, Kim J, Jung S, Woodside B, Luheshi GN (2014) Role of brain transmigrating neutrophils in depression-like behavior during systemic infection. Mol Psychiatry 19:599–606 Bohatschek M, Werner A, Raivich G (2001) Systemic LPS injection leads to granulocyte influx into normal and injured brain: effects of ICAM-1 deficiency. Exp Neurol 172:137–152 Ji KA, Eu MY, Kang SH, Gwag BJ, Jou I, Joe EH (2008) Differential neutrophil infiltration contributes to regional differences in brain inflammation in the substantia nigra pars compacta and cortex. Glia 56:1039–1047 Ji KA, Yang MS, Jeong HK, Min KJ, Kang SH, Jou I, Joe EH (2007) Resident microglia die and infiltrated neutrophils and monocytes become major inflammatory cells in lipopolysaccharide-injected brain. Glia 55:1577–1588 Rummel C, Inoue W, Poole S, Luheshi GN (2010) Leptin regulates leukocyte recruitment into the brain following systemic LPS-induced inflammation. Mol Psychiatry 15:523–534 Zhou H, Andonegui G, Wong CH, Kubes P (2009) Role of endothelial TLR4 for neutrophil recruitment into central nervous system microvessels in systemic inflammation. J Immunol 183:5244–5250 Rummel C, Bredehoft J, Damm J, Schweighofer H, Peek V, Harden LM (2016) Obesity impacts fever and sickness behavior during acute systemic inflammation. Physiology 31:117–130 Aguilar-Valles A, Inoue W, Rummel C, Luheshi GN (2015) Obesity, adipokines and neuroinflammation. Neuropharmacology 96:124–134