Microglia mediate postoperative hippocampal inflammation and cognitive decline in mice

JCI Insight

Volumn 2, Issue 7, 2017, Pages

  Feng, Xiaomei ^a   Valdearcos, Martin ^b   Uchida, Yosuke ^a   Lutrin, David ^a   Maze, Mervyn ^a   Koliwad, Suneil K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85021378138     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.91229     Document Type: Article

References (45)

1. Steinmetz J, Christensen KB, Lund T, Lohse N, Rasmussen LS, ISPOCD Group. Long-term consequences of postoperative cognitive dysfunction. Anesthesiology. 2009;110(3):548–555.
2. Crocker E, et al. Long-Term Effects of Postoperative Delirium in Patients Undergoing Cardiac Operation: A Systematic Review. Ann Thorac Surg. 2016;102(4):1391–1399.
3. Vacas S, Degos V, Feng X, Maze M. The neuroinflammatory response of postoperative cognitive decline. Br Med Bull. 2013;106:161–178.
4. Hirsch J, et al. Perioperative cerebrospinal fluid and plasma inflammatory markers after orthopedic surgery. J Neuroinflammation. 2016;13(1):211.
5. Ransohoff RM. How neuroinflammation contributes to neurodegeneration. Science. 2016;353(6301):777–783.
6. Wan Y, Xu J, Ma D, Zeng Y, Cibelli M, Maze M. Postoperative impairment of cognitive function in rats: a possible role for cytokine-mediated inflammation in the hippocampus. Anesthesiology. 2007;106(3):436–443.
7. Cibelli M, et al. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann Neurol. 2010;68(3):360–368.
8. Terrando N, Monaco C, Ma D, Foxwell BM, Feldmann M, Maze M. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc Natl Acad Sci USA. 2010;107(47):20518–20522.
9. Rosczyk HA, Sparkman NL, Johnson RW. Neuroinflammation and cognitive function in aged mice following minor surgery. Exp Gerontol. 2008;43(9):840–846.
10. O’Connor T, Borsig L, Heikenwalder M. CCL2-CCR2 Signaling in Disease Pathogenesis. Endocr Metab Immune Disord Drug Targets. 2015;15(2):105–118.
11. Terrando N, et al. Resolving postoperative neuroinflammation and cognitive decline. Ann Neurol. 2011;70(6):986–995.
12. Vacas S, Degos V, Tracey KJ, Maze M. High-mobility group box 1 protein initiates postoperative cognitive decline by engaging bone marrow-derived macrophages. Anesthesiology. 2014;120(5):1160–1167.
13. Degos V, et al. Depletion of bone marrow-derived macrophages perturbs the innate immune response to surgery and reduces postoperative memory dysfunction. Anesthesiology. 2013;118(3):527–536.
14. Butovsky O, et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci. 2014;17(1):131–143.
15. Valdearcos M, Xu AW, Koliwad SK. Hypothalamic inflammation in the control of metabolic function. Annu Rev Physiol. 2015;77:131–160.
16. McGrath KE, Frame JM, Palis J. Early hematopoiesis and macrophage development. Semin Immunol. 2015;27(6):379–387.
17. Li J, Chen K, Zhu L, Pollard JW. Conditional deletion of the colony stimulating factor-1 receptor (c-fms proto-oncogene) in mice. Genesis. 2006;44(7):328–335.
18. Elmore MR, et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron. 2014;82(2):380–397.
19. Erblich B, Zhu L, Etgen AM, Dobrenis K, Pollard JW. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS ONE. 2011;6(10):e26317.
20. Ginhoux F, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 2010;330(6005):841–845.
21. Dagher NN, et al. Colony-stimulating factor 1 receptor inhibition prevents microglial plaque association and improves cognition in 3xTg-AD mice. J Neuroinflammation. 2015;12:139.
22. Valdearcos M, Robblee MM, Benjamin DI, Nomura DK, Xu AW, Koliwad SK. Microglia dictate the impact of saturated fat consumption on hypothalamic inflammation and neuronal function. Cell Rep. 2014;9(6):2124–2138.
23. Spangenberg EE, Green KN. Inflammation in Alzheimer’s disease: Lessons learned from microglia-depletion models. Brain Behav Immun. 2017;61:1–11.
24. Feng X, et al. Surgery results in exaggerated and persistent cognitive decline in a rat model of the Metabolic Syndrome. Anesthesiology. 2013;118(5):1098–1105.
25. Poulos AM, et al. Conditioning- and time-dependent increases in context fear and generalization. Learn Mem. 2016;23(7):379–385.
26. Carlin LM, et al. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell. 2013;153(2):362–375.
27. Sharief MK, Thompson EJ. In vivo relationship of tumor necrosis factor-alpha to blood-brain barrier damage in patients with active multiple sclerosis. J Neuroimmunol. 1992;38(1-2):27–33.
28. Hudetz JA, Patterson KM, Iqbal Z, Gandhi SD, Pagel PS. Metabolic syndrome exacerbates short-term postoperative cognitive dysfunction in patients undergoing cardiac surgery: results of a pilot study. J Cardiothorac Vasc Anesth. 2011;25(2):282–287.
29. Monk TG, et al. Predictors of cognitive dysfunction after major noncardiac surgery. Anesthesiology. 2008;108(1):18–30.
30. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83(3):835–870.
31. Shinohara M, Serhan CN. Novel Endogenous Proresolving Molecules:Essential Fatty Acid-Derived and Gaseous Mediators in the Resolution of Inflammation. J Atheroscler Thromb. 2016;23(6):655–664.
32. Zhu YJ, Peng K, Meng XW, Ji FH. Attenuation of neuroinflammation by dexmedetomidine is associated with activation of a cholinergic anti-inflammatory pathway in a rat tibial fracture model. Brain Res. 2016;1644:1–8.
33. Hanisch UK. Microglia as a source and target of cytokines. Glia. 2002;40(2):140–155.
34. Langford D, Masliah E. Crosstalk between components of the blood brain barrier and cells of the CNS in microglial activation in AIDS. Brain Pathol. 2001;11(3):306–312.
35. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56.
36. Spite M, Clària J, Serhan CN. Resolvins, specialized proresolving lipid mediators, and their potential roles in metabolic diseases. Cell Metab. 2014;19(1):21–36.
37. Su X, et al. Dysfunction of inflammation-resolving pathways is associated with exaggerated postoperative cognitive decline in a rat model of the metabolic syndrome. Mol Med. 2013;18:1481–1490.
38. Fontaine DA, Davis DB. Attention to Background Strain Is Essential for Metabolic Research: C57BL/6 and the International Knockout Mouse Consortium. Diabetes. 2016;65(1):25–33.
39. Klegeris A, McGeer PL. Toxicity of human monocytic THP-1 cells and microglia toward SH-SY5Y neuroblastoma cells is reduced by inhibitors of 5-lipoxygenase and its activating protein FLAP. J Leukoc Biol. 2003;73(3):369–378.
40. Martini AC, et al. Lipoxin A4 inhibits microglial activation and reduces neuroinflammation and neuropathic pain after spinal cord hemisection. J Neuroinflammation. 2016;13(1):75.
41. Medeiros R, et al. Aspirin-triggered lipoxin A4 stimulates alternative activation of microglia and reduces Alzheimer disease-like pathology in mice. Am J Pathol. 2013;182(5):1780–1789.
42. Slade Shantz JA, Yu YY, Andres W, Miclau T, Marcucio R. Modulation of macrophage activity during fracture repair has differential effects in young adult and elderly mice. J Orthop Trauma. 2014;28 Suppl 1:S10–S14.
43. Butowski N, et al. Orally administered colony stimulating factor 1 receptor inhibitor PLX3397 in recurrent glioblastoma: an Ivy Foundation Early Phase Clinical Trials Consortium phase II study. Neuro-oncology. 2016;18(4):557–564.
44. Tap WD, et al. Structure-Guided Blockade of CSF1R Kinase in Tenosynovial Giant-Cell Tumor. N Engl J Med. 2015;373(5):428–437.
45. Hamilton JA, Cook AD, Tak PP. Anti-colony-stimulating factor therapies for inflammatory and autoimmune diseases. Nat Rev Drug Discov. 2016;16(1):53–70.