High-fat diet-induced brain region-specific phenotypic spectrum of CNS resident microglia

Acta Neuropathologica

Volumn 132, Issue 3, 2016, Pages 361-375

  Baufeld, Caroline ^a,b   Osterloh, Anja ^a   Prokop, Stefan ^a,c   Miller, Kelly R ^a,d   Heppner, Frank L ^a,e  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e BERLIN INSTITUTE OF HEALTH   (Germany)

Author keywords

Glia; High fat diet; Metabolism; Microglia

Indexed keywords

ARGINASE 1; CD74 ANTIGEN; CXCL1 CHEMOKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE TRANSPORTER 5; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPID; LIPOPOLYSACCHARIDE; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; TUMOR NECROSIS FACTOR;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE MARROW CELL; BRAIN; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; FEEDING; FEMALE; GENE EXPRESSION; GLIOSIS; HISTOPATHOLOGY; HUMAN; HYPOTHALAMUS; IN VIVO STUDY; LIPID DIET; LONG TERM EXPOSURE; MALE; MICROENVIRONMENT; MICROGLIA; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; ANIMAL; ANIMAL FOOD; C57BL MOUSE; CENTRAL NERVOUS SYSTEM; COMPLICATION; METABOLISM; NERVE CELL;

ANIMAL FEED; ANIMALS; ASTROCYTES; CENTRAL NERVOUS SYSTEM; DIET, HIGH-FAT; GLIOSIS; MALE; MICE, INBRED C57BL; MICROGLIA; NEURONS; OBESITY;

EID: 84978120874     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-016-1595-4     Document Type: Article

References (41)

1. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FMV (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
2. Ajmone-Cat MA, Mancini M, De Simone R, Cilli P, Minghetti L (2013) Microglial polarization and plasticity: evidence from organotypic hippocampal slice cultures. Glia 61:1698–1711. doi:10.1002/glia.22550
3. Ajmone-Cat MA, Nicolini A, Minghetti L (2003) Prolonged exposure of microglia to lipopolysaccharide modifies the intracellular signaling pathways and selectively promotes prostaglandin E2 synthesis. J Neurochem 87:1193–1203. doi:10.1046/j.1471-4159.2003.02087.x
4. Baquedano E, Ruiz-Lopez AM, Sustarsic EG, Herpy J, List EO, Chowen JA, Frago LM, Kopchick JJ, Argente J (2014) The absence of GH signaling affects the susceptibility to high-fat diet-induced hypothalamic inflammation in male mice. Endocrinology 155:4856–4867. doi:10.1210/en.2014-1367
5. Vom Berg J, Prokop S, Miller KR, Obst J, Kälin RE, Lopategui-Cabezas I, Wegner A, Mair F, Schipke CG, Peters O, Winter Y, Becher B, Heppner FL (2012) Inhibition of IL-12/IL-23 signaling reduces Alzheimer’s disease-like pathology and cognitive decline. Nat Med 18:1812–1819. doi:10.1038/nm.2965
6. Berrington de Gonzalez A, Hartge P, Cerhan JR, Flint AJ, Hannan L, MacInnis RJ, Moore SC, Tobias GS, Anton-Culver H, Freeman LB, Beeson WL, Clipp SL, English DR, Folsom AR, Freedman DM, Giles G, Hakansson N, Henderson KD, Hoffman-Bolton J, Hoppin JA, Koenig KL, Lee IM, Linet MS, Park Y, Pocobelli G, Schatzkin A, Sesso HD, Weiderpass E, Willcox BJ, Wolk A, Zeleniuch-Jacquotte A, Willett WC, Thun MJ (2010) Body-mass index and mortality among 1.46 million white adults. N Engl J Med 363:2211–2219. doi:10.1056/NEJMoa1000367
7. Boggs DA, Rosenberg L, Cozier YC, Wise LA, Coogan PF, Ruiz-Narvaez EA, Palmer JR (2011) General and abdominal obesity and risk of death among black women. N Engl J Med 365:901–908. doi:10.1056/NEJMoa1104119
8. Boitard C, Etchamendy N, Sauvant J, Aubert A, Tronel S, Marighetto A, Layé S, Ferreira G (2012) Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice. Hippocampus 22:2095–2100. doi:10.1002/hipo.22032
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. doi:10.1016/j.bbi.2013.06.007
10. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci 17:131–143. doi:10.1038/nn.3599
11. Chawla A, Nguyen KD, Goh YPS (2011) Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 11:738–749. doi:10.1038/nri3071
12. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334:292–295. doi:10.1056/NEJM199602013340503
13. Cunningham CL, Martínez-Cerdeño V, Noctor SC (2013) Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 33:4216–4233. doi:10.1523/JNEUROSCI.3441-12.2013
14. Enriori PJ, Evans AE, Sinnayah P, Jobst EE, Tonelli-Lemos L, Billes SK, Glavas MM, Grayson BE, Perello M, Nillni EA, Grove KL, Cowley MA (2007) Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab 5:181–194. doi:10.1016/j.cmet.2007.02.004
15. Fjeldborg K, Pedersen SB, Møller HJ, Christiansen T, Bennetzen M, Richelsen B (2014) Human adipose tissue macrophages are enhanced but changed to an anti-inflammatory profile in obesity. J Immunol Res 2014:309548. doi:10.1155/2014/309548
16. Frederich RC, Hamann A, Anderson S, Löllmann B, Lowell BB, Flier JS (1995) Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med 1:1311–1314. doi:10.1038/nm1295-1311
17. 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 C-X (2014) Hormones and diet, but not body weight, control hypothalamic microglial activity. Glia 62:17–25. doi:10.1002/glia.22580
18. Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang L, Means TK, El Khoury J (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16:1896–1905. doi:10.1038/nn.3554
19. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867. doi:10.1038/nature05485
20. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science (80-) 259:87–91
21. Hsuchou H, Kastin AJ, Pan W (2012) Blood-borne metabolic factors in obesity exacerbate injury-induced gliosis. J Mol Neurosci 47:267–277. doi:10.1007/s12031-012-9734-4
22. Jeon BT, Jeong EA, Shin HJ, Lee Y, Lee DH, Kim HJ, Kang SS, Cho GJ, Choi WS, Roh GS (2012) Resveratrol attenuates obesity-associated peripheral and central inflammation and improves memory deficit in mice fed a high-fat diet. Diabetes. doi:10.2337/db11-1498
23. Lampron A, Pimentel-Coelho PM, Rivest S (2013) Migration of bone marrow-derived cells into the central nervous system in models of neurodegeneration. J Comp Neurol 521:3863–3876. doi:10.1002/cne.23363
24. Lopes KO, Sparks DL, Streit WJ (2008) Microglial dystrophy in the aged and Alzheimer’s disease brain is associated with ferritin immunoreactivity. Glia 56:1048–1060. doi:10.1002/glia.20678
25. Mahad DJ, Ransohoff RM (2003) The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 15:23–32. doi:10.1016/S1044-5323(02)00125-2
26. Masuda T, Tsuda M, Yoshinaga R, Tozaki-Saitoh H, Ozato K, Tamura T, Inoue K (2012) IRF8 is a critical transcription factor for transforming microglia into a reactive phenotype. Cell Rep 1:334–340. doi:10.1016/j.celrep.2012.02.014
27. McNay DE, Briancon N, Kokoeva MV, Maratos-Flier E, Flier JS (2012) Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice. J Clin Invest 122:142–152. doi:10.1172/JCI43134
28. Milanski M, Degasperi G, Coope A, Morari J, Denis R, Cintra DE, Tsukumo DML, Anhe G, Amaral ME, Takahashi HK, Curi R, Oliveira HC, Carvalheira JBC, Bordin S, Saad MJ, Velloso LA (2009) Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J Neurosci 29:359–370. doi:10.1523/JNEUROSCI.2760-08.2009
29. Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR, Romanatto T, Carvalheira JB, Oliveira ALR, Saad MJ, Velloso LA (2009) High-fat diet induces apoptosis of hypothalamic neurons. PLoS One 4:e5045. doi:10.1371/journal.pone.0005045
30. 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. doi:10.1111/j.1365-2990.2012.01306.x
31. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR, Lafaille JJ, Hempstead BL, Littman DR, Gan W-B (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609. doi:10.1016/j.cell.2013.11.030
32. Perry VH, Holmes C (2014) Microglial priming in neurodegenerative disease. Nat Rev Neurol 10:217–224. doi:10.1038/nrneurol.2014.38
33. Streit WJ (2004) Microglia and Alzheimer’s disease pathogenesis. J Neurosci Res 77:1–8. doi:10.1002/jnr.20093
34. Streit WJ, Braak H, Xue Q-S, Bechmann I (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer’s disease. Acta Neuropathol 118:475–485. doi:10.1007/s00401-009-0556-6
35. Streit WJ, Xue Q-S, Tischer J, Bechmann I (2014) Microglial pathology. Acta Neuropathol Commun 2:142. doi:10.1186/s40478-014-0142-6
36. Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO, Zhao X, Sarruf DA, Izgur V, Maravilla KR, Nguyen HT, Fischer JD, Matsen ME, Wisse BE, Morton GJ, Horvath TL, Baskin DG, Tschop MH, Schwartz MW (2012) Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 122:153–162. doi:10.1172/JCI59660
37. Tran EH, Prince EN, Owens T (2000) IFN-gamma shapes immune invasion of the central nervous system via regulation of chemokines. J Immunol 164:2759–2768
38. Varvel NH, Grathwohl SA, Baumann F, Liebig C, Bosch A, Brawek B, Thal DR, Charo IF, Heppner FL, Aguzzi A, Garaschuk O, Ransohoff RM, Jucker M (2012) Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc Natl Acad Sci USA 109:18150–18155. doi:10.1073/pnas.1210150109
39. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808. doi:10.1172/JCI19246
40. Wyss-Coray T (2006) Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 12:1005–1015. doi:10.1038/nm1484
41. Zhang X, Zhang G, Zhang H, Karin M, Bai H, Cai D (2008) Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 135:61–73. doi:10.1016/j.cell.2008.07.043