Microglial Function during Glucose Deprivation: Inflammatory and Neuropsychiatric Implications

Molecular Neurobiology

Volumn 55, Issue 2, 2018, Pages 1477-1487

  Churchward, Matthew A ^a   Tchir, Devan R ^a   Todd, Kathryn G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Depression; Diabetes; Hypoglycemia; Inflammation; Ischemia; Microglia

Indexed keywords

INTERLEUKIN 1BETA; NITRIC OXIDE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL METABOLISM; CELL PROLIFERATION; COMORBIDITY; CONTROLLED STUDY; CYTOKINE RELEASE; DIABETES MELLITUS; GLUCOSE DEPRIVATION; GLUCOSE METABOLISM; IMMUNOFLUORESCENCE MICROSCOPY; INFLAMMATION; ISCHEMIA; MALE; MENTAL DISEASE; METABOLIC DISORDER; MICROGLIA; NEUROLOGIC DISEASE; NEUROPSYCHIATRY; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PHAGOCYTOSIS; RAT; SURVIVAL; ANIMAL; BRAIN; CELL CULTURE; HYPOGLYCEMIA; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN; CELL PROLIFERATION; CELLS, CULTURED; HYPOGLYCEMIA; INFLAMMATION; MICROGLIA; PHAGOCYTOSIS; RATS;

EID: 85011932327     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0422-9     Document Type: Article

References (119)

1. Heppner FL, Ransohoff RM, Becher B (2015) Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci 16:358–372. doi:10.1038/nrn3880
2. Prokop S, Miller KR, Heppner FL (2013) Microglia actions in Alzheimer’s disease. Acta Neuropathol (Berl) 126:461–477
3. Chao Y, Wong SC, Tan EK (2014) Evidence of inflammatory system involvement in Parkinson’s disease. Biomed Res Int 2014:308654. doi:10.1155/2014/308654
4. Deleidi M, Gasser T (2013) The role of inflammation in sporadic and familial Parkinson’s disease. Cell Mol Life Sci CMLS 70:4259–4273. doi:10.1007/s00018-013-1352-y
5. Soulet D, Cicchetti F (2011) The role of immunity in Huntington’s disease. Mol Psychiatry 16:889–902. doi:10.1038/mp.2011.28
6. Ahmad M, Dar NJ, Bhat ZS et al (2014) Inflammation in ischemic stroke: mechanisms, consequences and possible drug targets. CNS Neurol Disord Drug Targets 13:1378–1396
7. Jin R, Liu L, Zhang S et al (2013) Role of inflammation and its mediators in acute ischemic stroke. J Cardiovasc Transl Res 6:834–851. doi:10.1007/s12265-013-9508-6
8. Kim JY, Kawabori M, Yenari MA (2014) Innate inflammatory responses in stroke: mechanisms and potential therapeutic targets. Curr Med Chem 21:2076–2097
9. Kleinig TJ, Vink R (2009) Suppression of inflammation in ischemic and hemorrhagic stroke: therapeutic options. Curr Opin Neurol 22:294–301
10. Corps KN, Roth TL, McGavern DB (2015) Inflammation and neuroprotection in traumatic brain injury. JAMA Neurol 72:355–362. doi:10.1001/jamaneurol.2014.3558
11. Helmy A, De Simoni M-G, Guilfoyle MR et al (2011) Cytokines and innate inflammation in the pathogenesis of human traumatic brain injury. Prog Neurobiol 95:352–372. doi:10.1016/j.pneurobio.2011.09.003
12. Hinson HE, Rowell S, Schreiber M (2015) Clinical evidence of inflammation driving secondary brain injury: a systematic review. J Trauma Acute Care Surg 78:184–191. doi:10.1097/TA.0000000000000468
13. Zhou X, He X, Ren Y (2014) Function of microglia and macrophages in secondary damage after spinal cord injury. Neural Regen Res 9:1787–1795. doi:10.4103/1673-5374.143423
14. Roy A, Campbell MK (2013) A unifying framework for depression: bridging the major biological and psychosocial theories through stress. Clin Investig Med Médecine Clin Exp 36:E170–E190
15. Schiepers OJG, Wichers MC, Maes M (2005) Cytokines and major depression. Prog Neuro-Psychopharmacol Biol Psychiatry 29:201–217. doi:10.1016/j.pnpbp.2004.11.003
16. Zunszain PA, Hepgul N, Pariante CM (2013) Inflammation and depression. Curr Top Behav Neurosci 14:135–151. doi:10.1007/7854_2012_211
17. Feigenson KA, Kusnecov AW, Silverstein SM (2014) Inflammation and the two-hit hypothesis of schizophrenia. Neurosci Biobehav Rev 38:72–93. doi:10.1016/j.neubiorev.2013.11.006
18. Frick LR, Williams K, Pittenger C (2013) Microglial dysregulation in psychiatric disease. Clin Dev Immunol 2013:608654. doi:10.1155/2013/608654
19. Najjar S, Pearlman DM (2014) Neuroinflammation and white matter pathology in schizophrenia: systematic review. Schizophr Res. doi:10.1016/j.schres.2014.04.041
20. Watanabe Y, Someya T, Nawa H (2010) Cytokine hypothesis of schizophrenia pathogenesis: evidence from human studies and animal models. Psychiatry Clin Neurosci 64:217–230. doi:10.1111/j.1440-1819.2010.02094.x
21. Meyer U, Feldon J, Dammann O (2011) Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res 69:26R–33R. doi:10.1203/PDR.0b013e318212c196
22. Onore C, Careaga M, Ashwood P (2012) The role of immune dysfunction in the pathophysiology of autism. Brain Behav Immun 26:383–392. doi:10.1016/j.bbi.2011.08.007
23. Rossignol DA, Frye RE (2014) Evidence linking oxidative stress, mitochondrial dysfunction, and inflammation in the brain of individuals with autism. Front Physiol 5:150. doi:10.3389/fphys.2014.00150
24. Theoharides TC, Asadi S, Patel AB (2013) Focal brain inflammation and autism. J Neuroinflammation 10:46. doi:10.1186/1742-2094-10-46
25. Baker DG, Nievergelt CM, O’Connor DT (2012) Biomarkers of PTSD: neuropeptides and immune signaling. Neuropharmacology 62:663–673. doi:10.1016/j.neuropharm.2011.02.027
26. Wieck A, Grassi-Oliveira R, Hartmann do Prado C et al (2014) Neuroimmunoendocrine interactions in post-traumatic stress disorder: focus on long-term implications of childhood maltreatment. Neuroimmunomodulation 21:145–151. doi:10.1159/000356552
27. Rosenblat JD, Cha DS, Mansur RB, McIntyre RS (2014) Inflamed moods: a review of the interactions between inflammation and mood disorders. Prog Neuro-Psychopharmacol Biol Psychiatry. doi:10.1016/j.pnpbp.2014.01.013
28. Slavich GM, Irwin MR (2014) From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychol Bull 140:774–815. doi:10.1037/a0035302
29. Dowlati Y, Herrmann N, Swardfager W et al (2010) A meta-analysis of cytokines in major depression. Biol Psychiatry 67:446–457. doi:10.1016/j.biopsych.2009.09.033
30. Coulehan JL, Schulberg HC, Block MR et al (1990) Medical comorbidity of major depressive disorder in a primary medical practice. Arch Intern Med 150:2363–2367. doi:10.1001/archinte.1990.00390220099020
31. Jiang M, Qin P, Yang X (2014) Comorbidity between depression and asthma via immune-inflammatory pathways: a meta-analysis. J Affect Disord 166:22–29. doi:10.1016/j.jad.2014.04.027
32. Krishnan KRR, Delong M, Kraemer H et al (2002) Comorbidity of depression with other medical diseases in the elderly. Biol Psychiatry 52:559–588
33. Oladeji BD, Gureje O (2013) The comorbidity between depression and diabetes. Curr Psychiatry Rep 15:390. doi:10.1007/s11920-013-0390-3
34. Snyderman D, Wynn D (2009) Depression in cancer patients. Prim Care 36:703–719. doi:10.1016/j.pop.2009.07.008
35. Hanff TC, Furst SJ, Minor TR (2010) Biochemical and anatomical substrates of depression and sickness behavior. Isr J Psychiatry Relat Sci 47:64–71
36. Maes M, Berk M, Goehler L et al (2012) Depression and sickness behavior are Janus-faced responses to shared inflammatory pathways. BMC Med 10:66. doi:10.1186/1741-7015-10-66
37. Hauser P, Khosla J, Aurora H et al (2002) A prospective study of the incidence and open-label treatment of interferon-induced major depressive disorder in patients with hepatitis C. Mol Psychiatry 7:942–947. doi:10.1038/sj.mp.4001119
38. de Medeiros LPJ, Kayo M, Medeiros RBV et al (2014) Interferon-induced depression in patients with hepatitis C: an epidemiologic study. Rev Assoc Médica Bras 60:35–39 1992
39. Smith KJ, Norris S, McKiernan S et al (2012) An exploration of depressive symptoms in hepatitis C patients taking interferon-alpha: increase in sickness behaviors but not negative cognitions. J Clin Exp Hepatol 2:218–223. doi:10.1016/j.jceh.2012.03.001
40. Barakat R, Redzic Z (2015) The role of activated microglia and resident macrophages in the neurovascular unit during cerebral ischemia: is the jury still out? Med Princ Pract Int J Kuwait Univ Health Sci Cent. doi:10.1159/000435858
41. Morrison HW, Filosa JA (2013) A quantitative spatiotemporal analysis of microglia morphology during ischemic stroke and reperfusion. J Neuroinflammation 10:4. doi:10.1186/1742-2094-10-4
42. Morioka T, Kalehua AN, Streit WJ (1993) Characterization of microglial reaction after middle cerebral artery occlusion in rat brain. J Comp Neurol 327:123–132. doi:10.1002/cne.903270110
43. Zhang Z, Chopp M, Powers C (1997) Temporal profile of microglial response following transient (2 h) middle cerebral artery occlusion. Brain Res 744:189–198. doi:10.1016/S0006-8993(96)01085-2
44. Marks L, Carswell HV, Peters EE et al (2001) Characterization of the microglial response to cerebral ischemia in the stroke-prone spontaneously hypertensive rat. Hypertens Dallas Tex 38:116–122 1979
45. Loubinoux I, Kronenberg G, Endres M et al (2012) Post-stroke depression: mechanisms, translation and therapy. J Cell Mol Med 16:1961–1969. doi:10.1111/j.1582-4934.2012.01555.x
46. Taylor WD, Steffens DC, Krishnan KR (2006) Psychiatric disease in the twenty-first century: the case for subcortical ischemic depression. Biol Psychiatry 60:1299–1303. doi:10.1016/j.biopsych.2006.05.028
47. Thomas AJ, O’Brien JT, Davis S et al (2002) Ischemic basis for deep white matter hyperintensities in major depression: a neuropathological study. Arch Gen Psychiatry 59:785–792. doi:10.1001/archpsyc.59.9.785
48. Chui H (2001) Dementia due to subcortical ischemic vascular disease. Clin Cornerstone 3:40–51. doi:10.1016/S1098-3597(01)90047-X
49. Lee MJ, Seo SW, Na DL et al (2014) Synergistic effects of ischemia and β-amyloid burden on cognitive decline in patients with subcortical vascular mild cognitive impairment. JAMA Psychiatry 71:412–422. doi:10.1001/jamapsychiatry.2013.4506
50. Pluta R, Jolkkonen J, Cuzzocrea S et al (2011) Cognitive impairment with vascular impairment and degeneration. Curr Neurovasc Res 8:342–350
51. Villarreal AE, Barron R, Rao KS, Britton GB (2014) The effects of impaired cerebral circulation on Alzheimer’s disease pathology: evidence from animal studies. J Alzheimers Dis JAD 42:707–722. doi:10.3233/JAD-140144
52. Kim HA, Miller AA, Drummond GR et al (2012) Vascular cognitive impairment and Alzheimer’s disease: role of cerebral hypoperfusion and oxidative stress. Naunyn Schmiedeberg's Arch Pharmacol 385:953–959. doi:10.1007/s00210-012-0790-7
53. Pluta R, Furmaga-Jabłońska W, Maciejewski R et al (2013) Brain ischemia activates β- and γ-secretase cleavage of amyloid precursor protein: significance in sporadic Alzheimer’s disease. Mol Neurobiol 47:425–434. doi:10.1007/s12035-012-8360-z
54. Pluta R, Jabłoński M, Ułamek-Kozioł M et al (2013) Sporadic Alzheimer’s disease begins as episodes of brain ischemia and ischemically dysregulated Alzheimer’s disease genes. Mol Neurobiol 48:500–515. doi:10.1007/s12035-013-8439-1
55. McCrimmon RJ (2012) Update in the CNS response to hypoglycemia. J Clin Endocrinol Metab 97:1–8. doi:10.1210/jc.2011-1927
56. Berge LI, Riise T (2015) Comorbidity between type 2 diabetes and depression in the adult population: directions of the association and its possible pathophysiological mechanisms. Int J Endocrinol 2015:164760. doi:10.1155/2015/164760
57. Martinac M, Pehar D, Karlović D et al (2014) Metabolic syndrome, activity of the hypothalamic-pituitary-adrenal axis and inflammatory mediators in depressive disorder. Acta Clin Croat 53:55–71
58. Emanuele E, Martinelli V, Carlin MV et al (2011) Serum levels of soluble receptor for advanced glycation endproducts (sRAGE) in patients with different psychiatric disorders. Neurosci Lett 487:99–102. doi:10.1016/j.neulet.2010.10.003
59. Spauwen PJJ, van Eupen MGA, Köhler S et al (2015) Associations of advanced glycation end-products with cognitive functions in individuals with and without type 2 diabetes: the Maastricht Study. J Clin Endocrinol Metab 100:951–960. doi:10.1210/jc.2014-2754
60. Musen G, Lyoo IK, Sparks CR et al (2006) Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes 55:326–333
61. Tambuyzer BR, Ponsaerts P, Nouwen EJ (2009) Microglia: gatekeepers of central nervous system immunology. J Leukoc Biol 85:352–370. doi:10.1189/jlb.0608385
62. Katsumoto A, Lu H, Miranda AS, Ransohoff RM (2014) Ontogeny and functions of central nervous system macrophages. J Immunol Baltim Md 193:2615–2621. doi:10.4049/jimmunol.14007161950
63. Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15:300–312. doi:10.1038/nrn3722
64. Prinz M, Tay TL, Wolf Y, Jung S (2014) Microglia: unique and common features with other tissue macrophages. Acta Neuropathol (Berl) 128:319–331. doi:10.1007/s00401-014-1267-1
65. Schwartz M, Butovsky O, Brück W, Hanisch U-K (2006) Microglial phenotype: is the commitment reversible? Trends Neurosci 29:68–74. doi:10.1016/j.tins.2005.12.005
66. Boche D, Perry VH, Nicoll JAR (2013) Review: activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol 39:3–18. doi:10.1111/nan.12011
67. Town T, Nikolic V, Tan J (2005) The microglial “activation” continuum: from innate to adaptive responses. J Neuroinflammation 2:24. doi:10.1186/1742-2094-2-24
68. Raivich G (2005) Like cops on the beat: the active role of resting microglia. Trends Neurosci 28:571–573. doi:10.1016/j.tins.2005.09.001
69. Sierra A, Beccari S, Diaz-Aparicio I et al (2014) Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast 2014:610343. doi:10.1155/2014/610343
70. Tremblay M-È (2011) The role of microglia at synapses in the healthy CNS: novel insights from recent imaging studies. Neuron Glia Biol 7:67–76. doi:10.1017/S1740925X12000038
71. Zanier ER, Fumagalli S, Perego C et al (2015) Shape descriptors of the “never resting” microglia in three different acute brain injury models in mice. Intensive Care Med Exp 3:39. doi:10.1186/s40635-015-0039-0
72. Kroner A, Greenhalgh AD, Zarruk JG et al (2014) TNF and increased intracellular iron alter macrophage polarization to a detrimental M1 phenotype in the injured spinal cord. Neuron 83:1098–1116. doi:10.1016/j.neuron.2014.07.027
73. Morsch M, Radford R, Lee A et al (2015) In vivo characterization of microglial engulfment of dying neurons in the zebrafish spinal cord. Front Cell Neurosci 9:321. doi:10.3389/fncel.2015.00321
74. Schafer DP, Lehrman EK, Kautzman AG et al (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691–705. doi:10.1016/j.neuron.2012.03.026
75. Sierra A, Encinas JM, Deudero JJP et al (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495. doi:10.1016/j.stem.2010.08.014
76. Girard S, Brough D, Lopez-Castejon G et al (2013) Microglia and macrophages differentially modulate cell death after brain injury caused by oxygen-glucose deprivation in organotypic brain slices. Glia 61:813–824. doi:10.1002/glia.22478
77. Ajami B, Bennett JL, Krieger C et al (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538–1543. doi:10.1038/nn2014
78. Ajami B, Bennett JL, Krieger C et al (2011) Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14:1142–1149. doi:10.1038/nn.2887
79. Barakat R, Redzic Z (2015) Differential cytokine expression by brain microglia/macrophages in primary culture after oxygen glucose deprivation and their protective effects on astrocytes during anoxia. Fluids Barriers CNS 12:6. doi:10.1186/s12987-015-0002-1
80. Eyo U, Dailey ME (2012) Effects of oxygen-glucose deprivation on microglial mobility and viability in developing mouse hippocampal tissues. Glia 60:1747–1760. doi:10.1002/glia.22394
81. Hall AA, Leonardo CC, Collier LA et al (2009) Delayed treatments for stroke influence neuronal death in rat organotypic slice cultures subjected to oxygen glucose deprivation. Neuroscience 164:470–477. doi:10.1016/j.neuroscience.2009.08.051
82. Bell MT, Puskas F, Agoston VA et al (2013) Toll-like receptor 4-dependent microglial activation mediates spinal cord ischemia-reperfusion injury. Circulation 128:S152–S156. doi:10.1161/CIRCULATIONAHA.112.000024
83. Lalancette-Hébert M, Gowing G, Simard A et al (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27:2596–2605. doi:10.1523/JNEUROSCI.5360-06.2007
84. Montero M, González B, Zimmer J (2009) Immunotoxic depletion of microglia in mouse hippocampal slice cultures enhances ischemia-like neurodegeneration. Brain Res 1291:140–152. doi:10.1016/j.brainres.2009.06.097
85. Chen W, Ostrowski RP, Obenaus A, Zhang JH (2009) Prodeath or prosurvival: two facets of hypoxia inducible factor-1 in perinatal brain injury. Exp Neurol 216:7–15. doi:10.1016/j.expneurol.2008.10.016
86. Jantzie LL, Cheung P-Y, Todd KG (2005) Doxycycline reduces cleaved caspase-3 and microglial activation in an animal model of neonatal hypoxia-ischemia. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 25:314–324. doi:10.1038/sj.jcbfm.9600025
87. Lai AY, Todd KG (2006) Hypoxia-activated microglial mediators of neuronal survival are differentially regulated by tetracyclines. Glia 53:809–816. doi:10.1002/glia.20335
88. Shay JES, Celeste Simon M (2012) Hypoxia-inducible factors: crosstalk between inflammation and metabolism. Semin Cell Dev Biol 23:389–394. doi:10.1016/j.semcdb.2012.04.004
89. Choi SJ, Shin IJ, Je K-H et al (2013) Hypoxia antagonizes glucose deprivation on interleukin 6 expression in an Akt dependent, but HIF-1/2α independent manner. PLoS One 8:e58662. doi:10.1371/journal.pone.0058662
90. Eyo UB, Miner SA, Ahlers KE et al (2013) P2X7 receptor activation regulates microglial cell death during oxygen-glucose deprivation. Neuropharmacology 73:311–319. doi:10.1016/j.neuropharm.2013.05.032
91. Ziemka-Nałęcz M, Stanaszek L, Zalewska T (2013) Oxygen-glucose deprivation promotes gliogenesis and microglia activation in organotypic hippocampal slice culture: involvement of metalloproteinases. Acta Neurobiol Exp (Warsz) 73:130–142
92. Gimeno-Bayón J, López-López A, Rodríguez MJ, Mahy N (2014) Glucose pathways adaptation supports acquisition of activated microglia phenotype. J Neurosci Res 92:723–731. doi:10.1002/jnr.23356
93. Uhlemann R, Gertz K, Boehmerle W et al (2015) Actin dynamics shape microglia effector functions. Brain Struct Funct. doi:10.1007/s00429-015-1067-y
94. Orihuela R, McPherson CA, Harry GJ (2016) Microglial M1/M2 polarization and metabolic states. Br J Pharmacol 173:649–665. doi:10.1111/bph.13139
95. Saura J, Tusell JM, Serratosa J (2003) High-yield isolation of murine microglia by mild trypsinization. Glia 44:183–189. doi:10.1002/glia.10274
96. Tsikas D (2007) Analysis of nitrite and nitrate in biological fluids by assays based on the Griess reaction: appraisal of the Griess reaction in the L-arginine/nitric oxide area of research. J Chromatogr B Analyt Technol Biomed Life Sci 851:51–70. doi:10.1016/j.jchromb.2006.07.054
97. Griess P (1879) Bemerkungen zu der Abhandlung der HH. Weselsky und Benedikt,Ueber einige Azoverbindungen. Berichte Dtsch Chem Ges 12:426–428. doi:10.1002/cber.187901201117
98. Khatchadourian A, Bourque SD, Richard VR et al (2012) Dynamics and regulation of lipid droplet formation in lipopolysaccharide (LPS)-stimulated microglia. Biochim Biophys Acta 1821:607–617. doi:10.1016/j.bbalip.2012.01.007
99. Churchward MA, Todd KG (2014) Statin treatment affects cytokine release and phagocytic activity in primary cultured microglia through two separable mechanisms. Mol Brain 7:85. doi:10.1186/s13041-014-0085-7
100. Berridge MV, Tan AS (1993) Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303:474–482. doi:10.1006/abbi.1993.1311
101. Berridge MV, Herst PM, Tan AS (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev 11:127–152. doi:10.1016/S1387-2656(05)11004-7
102. Cabodevilla AG, Sánchez-Caballero L, Nintou E et al (2013) Cell survival during complete nutrient deprivation depends on lipid droplet-fueled β-oxidation of fatty acids. J Biol Chem 288:27777–27788. doi:10.1074/jbc.M113.466656
103. Tremblay M-E, Zhang I, Bisht K et al (2016) Remodeling of lipid bodies by docosahexaenoic acid in activated microglial cells. J Neuroinflammation 13:116. doi:10.1186/s12974-016-0580-0
104. Gasparovic C, Rosenberg GA, Wallace JA et al (2001) Magnetic resonance lipid signals in rat brain after experimental stroke correlate with neutral lipid accumulation. Neurosci Lett 301:87–90. doi:10.1016/S0304-3940(01)01616-0
105. Adibhatla RM, Hatcher JF (2010) Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 12:125–169. doi:10.1089/ARS.2009.2668
106. Yuan Y, Li P, Ye J (2012) Lipid homeostasis and the formation of macrophage-derived foam cells in atherosclerosis. Protein Cell 3:173–181. doi:10.1007/s13238-012-2025-6
107. Saunders DE, Howe FA, van den Boogaart A et al (1997) Discrimination of metabolite from lipid and macromolecule resonances in cerebral infarction in humans using short echo proton spectroscopy. J Magn Reson Imaging JMRI 7:1116–1121
108. Infantino V, Convertini P, Cucci L et al (2011) The mitochondrial citrate carrier: a new player in inflammation. Biochem J 438:433–436. doi:10.1042/BJ20111275
109. Mills EL, Kelly B, Logan A et al (2016) Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell 167:457–470.e13. doi:10.1016/j.cell.2016.08.064
110. Krawczyk CM, Holowka T, Sun J et al (2010) Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115:4742–4749. doi:10.1182/blood-2009-10-249540
111. Chang C-H, Curtis JD, Maggi LB et al (2013) Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153:1239–1251. doi:10.1016/j.cell.2013.05.016
112. O’Neill LAJ, Kishton RJ, Rathmell J (2016) A guide to immunometabolism for immunologists. Nat Rev Immunol 16:553–565. doi:10.1038/nri.2016.70
113. Crotti A, Ransohoff RM (2016) Microglial physiology and pathophysiology: insights from genome-wide transcriptional profiling. Immunity 44:505–515. doi:10.1016/j.immuni.2016.02.013
114. Casano AM, Peri F (2015) Microglia: multitasking specialists of the brain. Dev Cell 32:469–477. doi:10.1016/j.devcel.2015.01.018
115. Koponen H, Kautiainen H, Leppänen E et al (2015) Association between suicidal behaviour and impaired glucose metabolism in depressive disorders. BMC Psychiatry 15:163. doi:10.1186/s12888-015-0567-x
116. Mansur RB, Brietzke E, McIntyre RS (2015) Is there a “metabolic-mood syndrome”? A review of the relationship between obesity and mood disorders. Neurosci Biobehav Rev 52:89–104. doi:10.1016/j.neubiorev.2014.12.017
117. Pan A, Keum N, Okereke OI et al (2012) Bidirectional association between depression and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Diabetes Care 35:1171–1180. doi:10.2337/dc11-2055
118. Baek JH, Kang E-S, Fava M et al (2014) Serum lipids, recent suicide attempt and recent suicide status in patients with major depressive disorder. Prog Neuro-Psychopharmacol Biol Psychiatry 51:113–118. doi:10.1016/j.pnpbp.2014.01.018
119. da Graça CM, Nardin P, Buffon A et al (2014) Serum triglycerides, but not cholesterol or leptin, are decreased in suicide attempters with mood disorders. J Affect Disord 172C:403–409. doi:10.1016/j.jad.2014.10.033