Advertisement

Metabolic Brain Disease

, Volume 33, Issue 3, pp 615–635 | Cite as

The possible factors affecting microglial activation in cases of obesity with cognitive dysfunction

  • Titikorn Chunchai
  • Nipon Chattipakorn
  • Siriporn C. Chattipakorn
Review Article

Abstract

Obesity has reached epidemic proportions in many countries around the world. Several studies have reported that obesity can lead to the development of cognitive decline. There is increasing evidence to demonstrate that microglia play a crucial role in cognitive decline in cases of obesity, Alzheimer’s disease and also in the aging process. Although there have been several studies into microglia over the past decades, the mechanistic link between microglia and cognitive decline in obese models is still not fully understood. In this review, the current available evidence from both in vitro and in vivo investigations regarding the association between the alteration in microglial activity in different obese models with respect to cognition are included. The metabolite profiles from obesity, adiposity, dietary and hormone affected microglial activation and its function in the brain are comprehensively summarized. In addition, the possible roles of microglial activation in relation to cognitive dysfunction are also presented and discussed. To ensure a balanced perspective controversial reports regarding these issues are included and discussed.

Keywords

Microglia Obesity Cognitive function 

Notes

Acknowledgements

The authors thank Ms. Maria Love for her editorial assistance of this manuscript.

This work was supported by the Thailand Research Fund (RTA 6080003: SCC); the Royal Golden Jubilee PhD program (PHD/0146/2558 TC&SC); a NSTDA Research Chair Grant from the National Science and Technology Development Agency Thailand (NC) and a Chiang Mai University Center of Excellence Award (NC).

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. Anderberg RH, Richard JE, Eerola K, López-Ferreras L, Banke E, Hansson C, Nissbrandt H, Berqquist F, Gribble FM, Reimann F, Wernstedt Asterholm I, Lamy CM, Skibicka KP (2017) Glucagon-like Peptide-1 and its analogues act in the dorsal raphe and modulate central serotonin to reduce appetite and body weight. Diabetes 66(4):1062–1073.  https://doi.org/10.2337/db16-0755 CrossRefPubMedGoogle Scholar
  2. Andre C et al (2017) Inhibiting microglia expansion prevents diet-induced hypothalamic and peripheral inflammation. Diabetes 66:908–919.  https://doi.org/10.2337/db16-0586 CrossRefPubMedGoogle Scholar
  3. Balland E, Cowley MA (2015) New insights in leptin resistance mechanisms in mice. Front Neuroendocrinol 39:59–65.  https://doi.org/10.1016/j.yfrne.2015.09.004 CrossRefPubMedGoogle Scholar
  4. Bellavance MA, Rivest S (2014) The HPA - immune Axis and the Immunomodulatory actions of glucocorticoids in the brain. Front Immunol 5:136.  https://doi.org/10.3389/fimmu.2014.00136 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bell-Temin H, Culver-Cochran AE, Chaput D, Carlson CM, Kuehl M, Burkhardt BR, Bickford PC, Liu B, Stevens SM Jr (2015) Novel molecular insights into classical and alternative activation states of microglia as revealed by stable isotope labeling by amino acids in cell culture (SILAC)-based proteomics. Mol. Cell. Proteomics 14:3173–3184.  https://doi.org/10.1074/mcp.M115.053926 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bocarsly ME, Fasolino M, Kane GA, LaMarca EA, Kirschen GW, Karatsoreos IN, McEwen BS, Gould E (2015) Obesity diminishes synaptic markers, alters microglial morphology, and impairs cognitive function. Proc Natl Acad Sci U S A 112(51):15731–15736.  https://doi.org/10.1073/pnas.1511593112 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Boden G (2008) Obesity and free fatty acids. Endocrinol Metab Clin N Am 37:635–646, viii-ix.  https://doi.org/10.1016/j.ecl.2008.06.007 CrossRefGoogle Scholar
  8. Brocca ME, Pietranera L, Meyer M, Lima A, Roig P, de Kloet ER, De Nicola AF (2017) Mineralocorticoid receptor associates with pro-inflammatory bias in hippocampus of spontaneously hypertensive rats. J Neuroendocrinol 29(7).  https://doi.org/10.1111/jne.12489
  9. Buckman LB, Hasty AH, Flaherty DK, Buckman CT, Thompson MM, Matlock BK, Weller K, Ellacott KLJ (2014) Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav Immun 35:33–42.  https://doi.org/10.1016/j.bbi.2013.06.007 CrossRefPubMedGoogle Scholar
  10. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761–1772.  https://doi.org/10.2337/db06-1491 CrossRefPubMedGoogle Scholar
  11. Chhor V, le Charpentier T, Lebon S, Oré MV, Celador IL, Josserand J, Degos V, Jacotot E, Hagberg H, Sävman K, Mallard C, Gressens P, Fleiss B (2013) Characterization of phenotype markers and neuronotoxic potential of polarised primary microglia in vitro. Brain Behav Immun 32:70–85.  https://doi.org/10.1016/j.bbi.2013.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chunchai T, Samniang B, Sripetchwandee J, Pintana H, Pongkan W, Kumfu S, Shinlapawittayatorn K, KenKnight BH, Chattipakorn N, Chattipakorn SC (2016) Vagus nerve stimulation exerts the Neuroprotective effects in obese-insulin resistant rats, leading to the improvement of cognitive function. Sci Rep 6:26866.  https://doi.org/10.1038/srep26866 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Clegg DJ, Gotoh K, Kemp C, Wortman MD, Benoit SC, Brown LM, D'Alessio D, Tso P, Seeley RJ, Woods SC (2011) Consumption of a high-fat diet induces central insulin resistance independent of adiposity. Physiol Behav 103:10–16.  https://doi.org/10.1016/j.physbeh.2011.01.010 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Collaboration NCDRF (2016) Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet 387:1377–1396.  https://doi.org/10.1016/S0140-6736(16)30054-X CrossRefGoogle Scholar
  15. Davies DS, Ma J, Jegathees T, Goldsbury AC (2016) Microglia show altered morphology and reduced arborisation in human brain during aging and Alzheimer's disease. Brain Pathol 27(6):795–808.  https://doi.org/10.1111/bpa.12456 CrossRefPubMedGoogle Scholar
  16. Dey A, Hao S, Erion JR, Wosiski-Kuhn M, Stranahan AM (2014) Glucocorticoid sensitization of microglia in a genetic mouse model of obesity and diabetes. J Neuroimmunol 269:20–27.  https://doi.org/10.1016/j.jneuroim.2014.01.013 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Drake C, Boutin H, Jones MS, Denes A, McColl BW, Selvarajah JR, Hulme S, Georgiou RF, Hinz R, Gerhard A, Vail A, Prenant C, Julyan P, Maroy R, Brown G, Smigova A, Herholz K, Kassiou M, Crossman D, Francis S, Proctor SD, Russell JC, Hopkins SJ, Tyrrell PJ, Rothwell NJ, Allan SM (2011) Brain inflammation is induced by co-morbidities and risk factors for stroke. Brain Behav Immun 25:1113–1122.  https://doi.org/10.1016/j.bbi.2011.02.008 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Duffy CM, Xu H, Nixon JP, Bernlohr DA, Butterick TA (2017) Identification of a fatty acid binding protein4-UCP2 axis regulating microglial mediated neuroinflammation. Mol Cell Neurosci 80:52–57.  https://doi.org/10.1016/j.mcn.2017.02.004 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ebrahimi M, Heidari-Bakavoli AR, Shoeibi S, Mirhafez SR, Moohebati M, Esmaily H, Ghazavi H, Saberi Karimian M, Parizadeh SMR, Mohammadi M, Mohaddes Ardabili H, Ferns GA, Ghayour-Mobarhan M (2016) Association of Serum hs-CRP levels with the presence of obesity, diabetes mellitus, and other cardiovascular risk factors. J Clin Lab Anal 30:672–676.  https://doi.org/10.1002/jcla.21920 CrossRefPubMedGoogle Scholar
  20. Erion JR, Wosiski-Kuhn M, Dey A, Hao S, Davis CL, Pollock NK, Stranahan AM (2014) Obesity elicits interleukin 1-mediated deficits in hippocampal synaptic plasticity. J Neurosci 34:2618–2631.  https://doi.org/10.1523/JNEUROSCI.4200-13.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Feng X, Valdearcos M, Uchida Y, Lutrin D, Maze M, Koliwad SK (2017) Microglia mediate postoperative hippocampal inflammation and cognitive decline in mice. JCI Insight 2(7):e91229.  https://doi.org/10.1172/jci.insight.91229 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fernandes JT, Chutna O, Chu V, Conde JP, Outeiro TF (2016) A novel microfluidic cell co-culture platform for the study of the molecular mechanisms of Parkinson's disease and other Synucleinopathies. Front Neurosci 10:511.  https://doi.org/10.3389/fnins.2016.00511 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Franco R, Fernandez-Suarez D (2015) Alternatively activated microglia and macrophages in the central nervous system. Prog Neurobiol 131:65–86.  https://doi.org/10.1016/j.pneurobio.2015.05.003 CrossRefPubMedGoogle Scholar
  24. Freeman LR, Small BJ, Bickford PC, Umphlet C, Granholm AC (2011) A high-fat/high-cholesterol diet inhibits growth of fetal hippocampal transplants via increased inflammation. Cell Transplant 20:1499–1514.  https://doi.org/10.3727/096368910X557281 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Frei K, Siepl C, Groscurth P, Bodmer S, Schwerdel C, Fontana A (1987) Antigen presentation and tumor cytotoxicity by interferon-gamma-treated microglial cells. Eur J Immunol 17:1271–1278.  https://doi.org/10.1002/eji.1830170909 CrossRefPubMedGoogle Scholar
  26. Gao Y, Ottaway N, Schriever SC, Legutko B, García-Cáceres C, de la Fuente E, Mergen C, Bour S, Thaler JP, Seeley RJ, Filosa J, Stern JE, Perez-Tilve D, Schwartz MW, Tschöp MH, Yi CX (2014) Hormones and diet, but not body weight, control hypothalamic microglial activity. Glia 62:17–25.  https://doi.org/10.1002/glia.22580 CrossRefPubMedGoogle Scholar
  27. Ginhoux F, Prinz M (2015) Origin of microglia: current concepts and past controversies. Cold Spring Harb Perspect Biol 7:a020537.  https://doi.org/10.1101/cshperspect.a020537 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ginhoux F, Lim S, Hoeffel G, Low D, Huber T (2013) Origin and differentiation of microglia. Front Cell Neurosci 7:45.  https://doi.org/10.3389/fncel.2013.00045 CrossRefPubMedPubMedCentralGoogle Scholar
  29. de Git KC, Adan RA (2015) Leptin resistance in diet-induced obesity: the role of hypothalamic inflammation. Obes Rev 16(3):207–224.  https://doi.org/10.1111/obr.12243 CrossRefPubMedGoogle Scholar
  30. Grayson BE, Levasseur PR, Williams SM, Smith MS, Marks DL, Grove KL (2010) Changes in Melanocortin expression and inflammatory pathways in fetal offspring of nonhuman primates fed a high-fat diet. Endocrinology 151:1622–1632.  https://doi.org/10.1210/en.2009-1019 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Greenwood CE, Winocur G (2005) High-fat diets, insulin resistance and declining cognitive function. Neurobiol Aging 26(Suppl 1):42–45.  https://doi.org/10.1016/j.neurobiolaging.2005.08.017 CrossRefPubMedGoogle Scholar
  32. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140–155.  https://doi.org/10.1002/glia.10161 CrossRefPubMedGoogle Scholar
  33. Hao S, Dey A, Yu X, Stranahan AM (2016) Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun 51:230–239.  https://doi.org/10.1016/j.bbi.2015.08.023 CrossRefPubMedGoogle Scholar
  34. Hazama GI, Yasuhara O, Morita H, Aimi Y, Tooyama I, Kimura H (2005) Mouse brain IgG-like immunoreactivity: strain-specific occurrence in microglia and biochemical identification of IgG. J Comp Neurol 492:234–249.  https://doi.org/10.1002/cne.20710 CrossRefPubMedGoogle Scholar
  35. Hsuchou H, Kastin AJ, Pan W (2012) Blood-borne metabolic factors in obesity exacerbate injury-induced gliosis. J Mol Neurosci 47:267–277.  https://doi.org/10.1007/s12031-012-9734-4 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hwang IK, Kim IY, Kim YN, Yi SS, Park IS, Min BH, Doo HK, Ahn SY, Kim YS, Lee IS, Yoon YS, Seong JK (2009) Comparative study on high fat diet-induced 4-hydroxy-2E-nonenal adducts in the hippocampal CA1 region of C57BL/6N and C3H/HeN mice. Neurochem Res 34:964–972.  https://doi.org/10.1007/s11064-008-9846-y CrossRefPubMedGoogle Scholar
  37. Inoue K, Sakuma E, Morimoto H, Asai H, Koide Y, Leng T, Wada I, Xiong ZG, Ueki T (2016) Serum- and glucocorticoid-inducible kinases in microglia. Biochem Biophys Res Commun 478:53–59.  https://doi.org/10.1016/j.bbrc.2016.07.094 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Inoue T, Tanaka M, Masuda S, Ohue-Kitano R, Yamakage H, Muranaka K, Wada H, Kusakabe T, Shimatsu A, Hasegawa K, Satoh-Asahara N (2017) Omega-3 polyunsaturated fatty acids suppress the inflammatory responses of lipopolysaccharide-stimulated mouse microglia by activating SIRT1 pathways. Biochim Biophys Acta 1862(5):552–560.  https://doi.org/10.1016/j.bbalip.2017.02.010
  39. Iwai T, Ito S, Tanimitsu K, Udagawa S, Oka J (2006) Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes. Neurosci Res 55:352–360.  https://doi.org/10.1016/j.neures.2006.04.008 CrossRefPubMedGoogle Scholar
  40. Kahn SE, Hull RL, Utzschneider KM (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444:840–846.  https://doi.org/10.1038/nature05482 CrossRefPubMedGoogle Scholar
  41. Kappe C, Tracy LM, Patrone C, Iverfeldt K, Sjöholm Å (2012) GLP-1 secretion by microglial cells and decreased CNS expression in obesity. J Neuroinflammation 9:276.  https://doi.org/10.1186/1742-2094-9-276 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kettenmann H, Kirchhoff F, Verkhratsky A (2013) Microglia: new roles for the synaptic stripper. Neuron 77:10–18.  https://doi.org/10.1016/j.neuron.2012.12.023 CrossRefPubMedGoogle Scholar
  43. Kim YJ, Hwang SY, Oh ES, Oh S, Han IO (2006) IL-1beta, an immediate early protein secreted by activated microglia, induces iNOS/NO in C6 astrocytoma cells through p38 MAPK and NF-kappaB pathways. J Neurosci Res 84:1037–1046.  https://doi.org/10.1002/jnr.21011 CrossRefPubMedGoogle Scholar
  44. Kim KA, Gu W, Lee IA, Joh EH, Kim DH (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 7:e47713.  https://doi.org/10.1371/journal.pone.0047713 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kim HJ, Cho MH, Shim WH, Kim JK, Jeon EY, Kim DH, Yoon SY (2016) Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects. Mol Psychiatry 22(11):1576–1584.  https://doi.org/10.1038/mp.2016.103 CrossRefPubMedPubMedCentralGoogle Scholar
  46. de Kloet AD, Pati D, Wang L, Hiller H, Sumners C, Frazier CJ, Seeley RJ, Herman JP, Woods SC, Krause EG (2013) Angiotensin type 1a receptors in the paraventricular nucleus of the hypothalamus protect against diet-induced obesity. J Neurosci 33:4825–4833.  https://doi.org/10.1523/JNEUROSCI.3806-12.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  47. de Kloet AD, Pioquinto DJ, Nguyen D, Wang L, Smith JA, Hiller H, Sumners C (2014) Obesity induces neuroinflammation mediated by altered expression of the renin-angiotensin system in mouse forebrain nuclei. Physiol Behav 136:31–38.  https://doi.org/10.1016/j.physbeh.2014.01.016 CrossRefPubMedGoogle Scholar
  48. Kvarta MD, Bradbrook KE, Dantrassy HM, Bailey AM, Thompson SM (2015) Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. J Neurophysiol 114:1713–1724.  https://doi.org/10.1152/jn.00359.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kwon YH, Kim J, Kim CS, Tu TH, Kim MS, Suk K, Kim DH, Lee BJ, Choi HS, Park T, Choi MS, Goto T, Kawada T, Ha TY, Yu R (2017) Hypothalamic lipid-laden astrocytes induce microglia migration and activation. FEBS Lett 591:1742–1751.  https://doi.org/10.1002/1873-3468.12691 CrossRefPubMedGoogle Scholar
  50. Lee JK, Chung J, Kannarkat GT, Tansey MG (2013) Critical role of regulator G-protein signaling 10 (RGS10) in modulating macrophage M1/M2 activation. PLoS One 8:e81785.  https://doi.org/10.1371/journal.pone.0081785 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lee JJ, Wang PW, Yang IH, Huang HM, Chang CS, CL W, Chuang JH (2015) High-fat diet induces toll-like receptor 4-dependent macrophage/microglial cell activation and retinal impairment. Invest Ophthalmol Vis Sci 56:3041–3050.  https://doi.org/10.1167/iovs.15-16504 CrossRefPubMedGoogle Scholar
  52. Lemus MB, Bayliss JA, Lockie SH, Santos VV, Reichenbach A, Stark R, Andrews ZB (2015) A stereological analysis of NPY, POMC, Orexin, GFAP astrocyte, and Iba1 microglia cell number and volume in diet-induced obese male mice. Endocrinology 156:1701–1713.  https://doi.org/10.1210/en.2014-1961 CrossRefPubMedGoogle Scholar
  53. Ma L, Allen M, Sakae N, Ertekin-Taner N, Graff-Radford NR, Dickson DW, Younkin SG, Sevlever D (2016) Expression and processing analyses of wild type and p.R47H TREM2 variant in Alzheimer's disease brains. Mol Neurodegener 11:72.  https://doi.org/10.1186/s13024-016-0137-9 CrossRefPubMedPubMedCentralGoogle Scholar
  54. McEwen HJ, Inglis MA, Quennell JH, Grattan DR, Anderson GM (2016) Deletion of suppressor of cytokine signaling 3 from forebrain neurons delays infertility and onset of hypothalamic Leptin resistance in response to a high caloric diet. J Neurosci: Off J Soc Neurosci 36:7142–7153.  https://doi.org/10.1523/JNEUROSCI.2714-14.2016 CrossRefGoogle Scholar
  55. Moehle MS, West AB (2015) M1 and M2 immune activation in Parkinson's disease: foe and ally? Neuroscience 302:59–73.  https://doi.org/10.1016/j.neuroscience.2014.11.018 CrossRefPubMedGoogle Scholar
  56. Moller K et al (2016) Influence of weight reduction on blood levels of C-reactive protein, tumor necrosis factor-alpha, interleukin-6, and oxylipins in obese subjects. Prostaglandins Leukot Essent Fat Acids 106:39–49.  https://doi.org/10.1016/j.plefa.2015.12.001 CrossRefGoogle Scholar
  57. Nayak D, Roth TL, McGavern DB (2014) Microglia development and function. Annu Rev Immunol 32:367–402.  https://doi.org/10.1146/annurev-immunol-032713-120240 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Neniskyte U, Vilalta A, Brown GC (2014) Tumour necrosis factor alpha-induced neuronal loss is mediated by microglial phagocytosis. FEBS Lett 588:2952–2956.  https://doi.org/10.1016/j.febslet.2014.05.046 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Norden DM, Trojanowski PJ, Villanueva E, Navarro E, Godbout JP (2016) Sequential activation of microglia and astrocyte cytokine expression precedes increased iba-1 or GFAP immunoreactivity following systemic immune challenge. Glia 64:300–316.  https://doi.org/10.1002/glia.22930 CrossRefPubMedGoogle Scholar
  60. Ouyang S, Hsuchou H, Kastin AJ, Wang Y, Yu C, Pan W (2014) Diet-induced obesity suppresses expression of many proteins at the blood-brain barrier. J Cereb Blood Flow Metab 34:43–51.  https://doi.org/10.1038/jcbfm.2013.166 CrossRefPubMedGoogle Scholar
  61. Pintana H, Apaijai N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2012) Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci 91:409–414.  https://doi.org/10.1016/j.lfs.2012.08.017 CrossRefPubMedGoogle Scholar
  62. Pipatpiboon N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2012) PPARgamma agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term high-fat diets. Endocrinology 153:329–338.  https://doi.org/10.1210/en.2011-1502 CrossRefPubMedGoogle Scholar
  63. Pipatpiboon N, Pintana H, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2013) DPP4-inhibitor improves neuronal insulin receptor function, brain mitochondrial function and cognitive function in rats with insulin resistance induced by high-fat diet consumption. Eur J Neurosci 37:839–849.  https://doi.org/10.1111/ejn.12088 CrossRefPubMedGoogle Scholar
  64. Pratchayasakul W, Kerdphoo S, Petsophonsakul P, Pongchaidecha A, Chattipakorn N, Chattipakorn SC (2011) Effects of high-fat diet on insulin receptor function in rat hippocampus and the level of neuronal corticosterone. Life Sci 88:619–627.  https://doi.org/10.1016/j.lfs.2011.02.003 CrossRefPubMedGoogle Scholar
  65. Pratchayasakul W, Sa-nguanmoo P, Sivasinprasasn S, Pintana H, Tawinvisan R, Sripetchwandee J, Kumfu S, Chattipakorn N, Chattipakorn SC (2015) Obesity accelerates cognitive decline by aggravating mitochondrial dysfunction, insulin resistance and synaptic dysfunction under estrogen-deprived conditions. Horm Behav 72:68–77.  https://doi.org/10.1016/j.yhbeh.2015.04.023 CrossRefPubMedGoogle Scholar
  66. Rachmany L, Tweedie D, Li Y, Rubovitch V, Holloway HW, Miller J, Hoffer BJ, Greig NH, Pick CG (2013) Exendin-4 induced glucagon-like peptide-1 receptor activation reverses behavioral impairments of mild traumatic brain injury in mice. Age (Dordr) 35:1621–1636.  https://doi.org/10.1007/s11357-012-9464-0 CrossRefGoogle Scholar
  67. Samniang B, Shinlapawittayatorn K, Chunchai T, Pongkan W, Kumfu S, Chattipakorn SC, KenKnight BH, Chattipakorn N (2016) Vagus nerve stimulation improves cardiac function by preventing mitochondrial dysfunction in obese-insulin resistant rats. Sci Rep 6:19749.  https://doi.org/10.1038/srep19749 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sa-Nguanmoo P et al (2016) FGF21 improves cognition by restored synaptic plasticity, dendritic spine density, brain mitochondrial function and cell apoptosis in obese-insulin resistant male rats. Horm Behav 85:86–95.  https://doi.org/10.1016/j.yhbeh.2016.08.006 CrossRefPubMedGoogle Scholar
  69. Sen T, Cawthon CR, Ihde BT, Hajnal A, DiLorenzo PM, de La Serre CB, Czaja K (2017) Diet-driven microbiota dysbiosis is associated with vagal remodeling and obesity. Physiol Behav 173:305–317.  https://doi.org/10.1016/j.physbeh.2017.02.027 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Smith JA, Das A, Ray SK, Banik NL (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res Bull 87:10–20.  https://doi.org/10.1016/j.brainresbull.2011.10.004 CrossRefPubMedGoogle Scholar
  71. Sripetchwandee J, Pipatpiboon N, Pratchayasakul W, Chattipakorn N, Chattipakorn SC (2014) DPP-4 inhibitor and PPARgamma agonist restore the loss of CA1 dendritic spines in obese insulin-resistant rats. Arch Med Res 45:547–552.  https://doi.org/10.1016/j.arcmed.2014.09.002 CrossRefPubMedGoogle Scholar
  72. Stence N, Waite M, Dailey ME (2001) Dynamics of microglial activation: a confocal time-lapse analysis in hippocampal slices. Glia 33:256–266.  https://doi.org/10.1002/1098-1136(200103)33:3<256::AID-GLIA1024>3.0.CO;2-J CrossRefPubMedGoogle Scholar
  73. Stienstra R, van Diepen JA, Tack CJ, Zaki MH, van de Veerdonk FL, Perera D, Neale GA, Hooiveld GJ, Hijmans A, Vroegrijk I, van den Berg S, Romijn J, Rensen PCN, Joosten LAB, Netea MG, Kanneganti TD (2011) Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci U S A 108:15324–15329.  https://doi.org/10.1073/pnas.1100255108 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, Egan JM, Mattson MP (2008) Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18:1085–1088.  https://doi.org/10.1002/hipo.20470 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Stranahan AM, Hao S, Dey A, Yu X, Baban B (2016) Blood-brain barrier breakdown promotes macrophage infiltration and cognitive impairment in leptin receptor-deficient mice. J Cereb Blood Flow Metab 36:2108–2121.  https://doi.org/10.1177/0271678X16642233 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Su F, Yi H, Xu L, Zhang Z (2015) Fluoxetine and S-citalopram inhibit M1 activation and promote M2 activation of microglia in vitro. Neuroscience 294:60–68.  https://doi.org/10.1016/j.neuroscience.2015.02.028 CrossRefPubMedGoogle Scholar
  77. Takahashi K, Rochford CD, Neumann H (2005) Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201:647–657.  https://doi.org/10.1084/jem.20041611 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tamargo IA, Bader M, Li Y, Yu SJ, Wang Y, Talbot K, DiMarchi RD, Pick CG, Greig NH (2016) Novel GLP-1R/GIPR co-agonist "twincretin" is neuroprotective in cell and rodent models of mild traumatic brain injury. Exp Neurol:176–186.  https://doi.org/10.1016/j.expneurol.2016.11.005
  79. Tang Y, Le W (2015) Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol 53:1181–1194.  https://doi.org/10.1007/s12035-014-9070-5 CrossRefPubMedGoogle Scholar
  80. Tentillier N, Etzerodt A, Olesen MN, Rizalar FS, Jacobsen J, Bender D, Moestrup SK, Romero-Ramos M (2016) Anti-inflammatory modulation of microglia via CD163-targeted glucocorticoids protects dopaminergic neurons in the 6-OHDA Parkinson's disease model. J Neurosci Off J Soc Neurosci 36:9375–9390.  https://doi.org/10.1523/JNEUROSCI.1636-16.2016 CrossRefGoogle Scholar
  81. Oh-I S, Thaler JP, Ogimoto K, Wisse BE, Morton GJ, Schwartz MW (2010) Central administration of interleukin-4 exacerbates hypothalamic inflammation and weight gain during high-fat feeding. AJP: Endocrinol Metab 299(1):E47–E53.  https://doi.org/10.1152/ajpendo.00026.2010 CrossRefGoogle Scholar
  82. Tracy LM, Bergqvist F, Ivanova EV, Jacobsen KT, Iverfeldt K (2013) Exposure to the saturated free fatty acid Palmitate alters BV-2 microglia inflammatory response. J Mol Neurosci 51:805–812.  https://doi.org/10.1007/s12031-013-0068-7 CrossRefPubMedGoogle Scholar
  83. Trang T, Beggs S, Salter MW (2011) Brain-derived neurotrophic factor from microglia: a molecular substrate for neuropathic pain. Neuron Glia Biol 7:99–108.  https://doi.org/10.1017/S1740925X12000087 CrossRefPubMedGoogle Scholar
  84. Tsunekawa T, Banno R, Mizoguchi A, Sugiyama M, Tominaga T, Onoue T, Hagiwara D, Ito Y, Iwama S, Goto M, Suga H, Sugimura Y, Arima H (2017) Deficiency of PTP1B attenuates hypothalamic inflammation via activation of the JAK2-STAT3 pathway in microglia. EBioMedicine 16:172–183.  https://doi.org/10.1016/j.ebiom.2017.01.007 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Ueno M, Fujita Y, Tanaka T, Nakamura Y, Kikuta J, Ishii M, Yamashita T (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543–551.  https://doi.org/10.1038/nn.3358 CrossRefPubMedGoogle Scholar
  86. Vaughn AC, Cooper EM, DiLorenzo PM, O'Loughlin LJ, Konkel ME, Peters JH, Hajnal A, Sen T, Lee SH, de la Serre CB, Czaja K (2017) Energy-dense diet triggers changes in gut microbiota, reorganization of gutbrain vagal communication and increases body fat accumulation. Acta Neurobiol Exp (Wars) 77:18–30Google Scholar
  87. Wake H, Moorhouse AJ, Miyamoto A, Nabekura J (2013) Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci 36:209–217.  https://doi.org/10.1016/j.tins.2012.11.007 CrossRefPubMedGoogle Scholar
  88. Wang Z, Liu D, Wang F, Liu S, Zhao S, Ling EA, Hao A (2012) Saturated fatty acids activate microglia via toll-like receptor 4/NF-kappaB signalling. Br J Nutr 107:229–241.  https://doi.org/10.1017/S0007114511002868 CrossRefPubMedGoogle Scholar
  89. Wang WY, Tan MS, JT Y, Tan L (2015) Role of pro-inflammatory cytokines released from microglia in Alzheimer's disease. Ann Transl Med 3:136.  https://doi.org/10.3978/j.issn.2305-5839.2015.03.49 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Wee YS, Weis JJ, Gahring LC, Rogers SW, Weis JH (2015) Age-related onset of obesity corresponds with metabolic Dysregulation and altered microglia morphology in mice deficient for Ifitm proteins. PLoS One 10:e0123218.  https://doi.org/10.1371/journal.pone.0123218 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, Tsui H, Wu P, Davidson MG, Alonso MN, Leong HX, Glassford A, Caimol M, Kenkel JA, Tedder TF, McLaughlin T, Miklos DB, Dosch HM, Engleman EG (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 17:610–617.  https://doi.org/10.1038/nm.2353 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Yang J, Kim CS, Tu T, Kim MS, Goto T, Kawada T, Choi MS, Park T, Sung MK, Yun J, Choe SY, Lee J, Joe Y, Choi HS, Back S, Chung H, Yu R (2017) Quercetin protects obesity-induced hypothalamic inflammation by reducing microglia-mediated inflammatory responses via HO-1 induction. Nutrients 9.  https://doi.org/10.3390/nu9070650
  93. Yi C-X, al-Massadi O, Donelan E, Lehti M, Weber J, Ress C, Trivedi C, Müller TD, Woods SC, Hofmann SM (2012a) Exercise protects against high-fat diet-induced hypothalamic inflammation. Physiol Behav 106:485–490.  https://doi.org/10.1016/j.physbeh.2012.03.021 CrossRefPubMedGoogle Scholar
  94. Yi CX, Tschop MH, Woods SC, Hofmann SM (2012b) High-fat-diet exposure induces IgG accumulation in hypothalamic microglia. Dis Model Mech 5:686–690.  https://doi.org/10.1242/dmm.009464 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Yuan L, Liu S, Bai X, Gao Y, Liu G, Wang X, Liu D, Li T, Hao A, Wang Z (2016) Oxytocin inhibits lipopolysaccharide-induced inflammation in microglial cells and attenuates microglial activation in lipopolysaccharide-treated mice. J Neuroinflammation 13:77.  https://doi.org/10.1186/s12974-016-0541-7 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Zhang QS, Heng Y, Yuan YH, Chen NH (2016) Pathological alpha-synuclein exacerbates the progression of Parkinson's disease through microglial activation. Toxicol Lett 265:30–37.  https://doi.org/10.1016/j.toxlet.2016.11.002 CrossRefPubMedGoogle Scholar
  97. Zhu C, Xu B, Sun X, Zhu Q, Sui Y (2016) Targeting CCR3 to reduce amyloid-beta production, tau hyperphosphorylation, and synaptic loss in a mouse model of Alzheimer's disease. Mol Neurobiol 54(10):7964–7978.  https://doi.org/10.1007/s12035-016-0269-5 CrossRefPubMedGoogle Scholar
  98. Zhuang P, Shou Q, Lu Y, Wang G, Qiu J, Wang J, He L, Chen J, Jiao J, Zhang Y (2017) Arachidonic acid sex-dependently affects obesity through linking gut microbiota-driven inflammation to hypothalamus-adipose-liver axis. Biochim Biophys Acta 1863:2715–2726.  https://doi.org/10.1016/j.bbadis.2017.07.003 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Titikorn Chunchai
    • 1
    • 2
  • Nipon Chattipakorn
    • 1
    • 2
  • Siriporn C. Chattipakorn
    • 1
    • 3
  1. 1.Neurophysiology Unit, Cardiac Electrophysiology Research and Training Center, Faculty of MedicineChiang Mai UniversityChiang MaiThailand
  2. 2.Cardiac Electrophysiology Research and Training Center, Department of Physiology, Faculty of MedicineChiang Mai UniversityChiang MaiThailand
  3. 3.Department of Oral Biology and Diagnostic Sciences, Faculty of DentistryChiang Mai UniversityChiang MaiThailand

Personalised recommendations