Calorie restriction attenuates lipopolysaccharide (LPS)-induced microglial activation in discrete regions of the hypothalamus and the subfornical organ

Brain, Behavior, and Immunity

Volumn 38, Issue , 2014, Pages 13-24

  Radler, Morgan E ^a   Hale, Matthew W ^a   Kent, Stephen ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

Calorie restriction; Diet; Dietary restriction; Fever; Food restriction; Iba1; Lipopolysaccharide; LPS; Microglia; Neuroinflammation

Indexed keywords

ADAPTOR PROTEIN; LIPOPOLYSACCHARIDE; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARCUATE NUCLEUS; ARTICLE; BLOOD BRAIN BARRIER; BODY TEMPERATURE; BRAIN REGION; CALCIUM BINDING; CALORIC RESTRICTION; CONTROLLED STUDY; DIET RESTRICTION; FEVER; HYPOTHALAMUS; IMMUNITY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRESS; SUBFORNICAL ORGAN; THALAMUS VENTRAL NUCLEUS; THERMOREGULATION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; HYPOTHALAMUS VENTROMEDIAL NUCLEUS;

ANIMALS; CALCIUM-BINDING PROTEINS; CALORIC RESTRICTION; HYPOTHALAMUS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; MICROGLIA; SUBFORNICAL ORGAN;

EID: 84898544656     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.11.014     Document Type: Article

References (96)

1. Anand B.K., Brobeck J.R. Localization of a "feeding center" in the hypothalamus of the rat. Proc. Soc. Exp. Biol. Med. 1951, 77(2):323-324. 10.3181/00379727-77-18766.
2. Bartfai T., Conti B. Molecules affecting hypothalamic control of core body temperature in response to calorie intake. Front. Genet. 2012, 3:184. 10.3389/fgene.2012.00184.
3. Benicky J., Sanchez-Lemus E., Honda M., Pang T., Orecna M., Wang J., Saavedra J.M. Angiotensin II AT1 receptor blockade ameliorates brain inflammation. Neuropsychopharmacology 2011, 36(4):857-870. 10.1038/npp.2010.225.
4. Beynon S.B., Walker F.R. Microglial activation in the injured and healthy brain: what are we really talking about? Practical and theoretical issues associated with the measurement of changes in microglial morphology. Neuroscience 2012, 225:162-171. 10.1016/j.neuroscience.2012.07.029.
5. Boche D., Perry V.H., Nicoll J.A. Review: activation patterns of microglia and their identification in the human brain. Neuropathol. Appl. Neurobiol. 2013, 39(1):3-18. 10.1111/nan.12011.
6. Borges B.C., Rorato R., Antunes-Rodrigues J., Elias L.L. Glial cell activity is maintained during prolonged inflammatory challenge in rats. Braz. J. Med. Biol. Res. 2012, 45(8):784-791. 10.1590/S0100-879X2012007500069.
7. Broberger C., Johansen J., Johansson C., Schalling M., Hokfelt T. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc. Natl. Acad. Sci. USA 1998, 95(25):15043-15048. 10.1073/pnas.95.25.15043.
8. Buchanan J.B., Sparkman N.L., Johnson R.W. Methamphetamine sensitization attenuates the febrile and neuroinflammatory response to a subsequent peripheral immune stimulus. Brain Behav. Immun. 2010, 24(3):502-511. 10.1016/j.bbi.2009.12.008.
9. Buttini M., Limonta S., Boddeke H.W. Peripheral administration of lipopolysaccharide induces activation of microglial cells in rat brain. Neurochem. Int. 1996, 29(1):25-35. [pii]. 10.1016/0197-0186(95)00141-7.
10. Carlini V.P., Martini A.C., Schioth H.B., Ruiz R.D., Fiol de Cuneo M., de Barioglio S.R. Decreased memory for novel object recognition in chronically food-restricted mice is reversed by acute ghrelin administration. Neuroscience 2008, 153(4):929-934. 10.1016/j.neuroscience.2008.03.015.
11. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389(6653):816-824. 10.1038/39807.
12. Chung D.W., Yoo K.Y., Hwang I.K., Kim D.W., Chung J.Y., Lee C.H., Won M.H. Systemic administration of lipopolysaccharide induces cyclooxygenase-2 immunoreactivity in endothelium and increases microglia in the mouse hippocampus. Cell. Mol. Neurobiol. 2010, 30(4):531-541. 10.1007/s10571-009-9477-0.
13. Colton C.A. Heterogeneity of microglial activation in the innate immune response in the brain. J. Neuroimmune Pharmacol. 2009, 4(4):399-418. 10.1007/s11481-009-9164-4.
14. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9(1):46-56. 10.1038/nrn2297.
15. Dong W., Selgrade M.K., Gilmour I.M., Lange R.W., Park P., Luster M.I., Kari F.W. Altered alveolar macrophage function in calorie-restricted rats. Am. J. Respir. Cell. Mol. Biol. 1998, 19(3):462-469. 10.1165/ajrcmb.19.3.3114.
16. Elmquist J.K., Coppari R., Balthasar N., Ichinose M., Lowell B.B. Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J. Comp. Neurol. 2005, 493(1):63-71. 10.1002/cne.20786.
17. Fan-xin M., Li-mei S., Bei S., Xin Q., Yu Y., Yu C. Heat shock factor 1 regulates the expression of the TRPV1 gene in the rat preoptic-anterior hypothalamus area during lipopolysaccharide-induced fever. Exp. Physiol. 2012, 97(6):730-740. 10.1113/expphysiol.2011.064204.
18. Felies M., von Horsten S., Pabst R., Nave H. Neuropeptide Y stabilizes body temperature and prevents hypotension in endotoxaemic rats. J. Physiol. 2004, 561:245-252. 10.1113/jphysiol.2004.073635.
19. Fenn A.M., Henry C.J., Huang Y., Dugan A., Godbout J.P. Lipopolysaccharide-induced interleukin (IL)-4 receptor-alpha expression and corresponding sensitivity to the M2 promoting effects of IL-4 are impaired in microglia of aged mice. Brain Behav. Immun. 2012, 26(5):766-777. 10.1016/j.bbi.2011.10.003.
20. Ferreira R., Xapelli S., Santos T., Silva A.P., Cristovao A., Cortes L., Malva J.O. Neuropeptide Y modulation of interleukin-1{beta} (IL-1{beta})-induced nitric oxide production in microglia. J. Biol. Chem. 2010, 285(53):41921-41934. 10.1074/jbc.M110.164020.
21. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 2005, Academic Press, San Diego. second ed.
22. Gordon C.J. Relationship between autonomic and behavioral thermoregulation in the mouse. Physiol. Behav. 1985, 34(5):687-690. 10.1016/0031-9384(85)90365-8.
23. Govic A., Levay E.A., Hazi A., Penman J., Kent S., Paolini A.G. Alterations in male sexual behaviour, attractiveness and testosterone levels induced by an adult-onset calorie restriction regimen. Behav. Brain Res. 2008, 190(1):140-146. 10.1016/j.bbr.2008.02.013.
24. Grayson B.E., Fitzgerald M.F., Hakala-Finch A.P., Ferris V.M., Begg D.P., Tong J., Benoit S.C. Improvements in hippocampal-dependent memory and microglial infiltration with calorie restriction and gastric bypass surgery, but not with vertical sleeve gastrectomy. Int. J. Obes. 2013, Epub ahead of print retrieved September 1. 10.1038/ijo.2013.100.
25. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
26. Halagappa V.K., Guo Z., Pearson M., Matsuoka Y., Cutler R.G., Laferla F.M., Mattson M.P. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 2007, 26(1):212-220. 10.1016/j.nbd.2006.12.019.
27. Hale M.W., Dady K.F., Evans A.K., Lowry C.A. Evidence for in vivo thermosensitivity of serotonergic neurons in the rat dorsal raphe nucleus and raphe pallidus nucleus implicated in thermoregulatory cooling. Exp. Neurol. 2011, 227(2):264-278. 10.1016/j.expneurol.2010.11.012.
28. Herber D.L., Maloney J.L., Roth L.M., Freeman M.J., Morgan D., Gordon M.N. Diverse microglial responses after intrahippocampal administration of lipopolysaccharide. Glia 2006, 53(4):382-391. 10.1002/glia.20272.
29. Hinwood M., Tynan R.J., Charnley J.L., Beynon S.B., Day T.A., Walker F.R. Chronic stress induced remodeling of the prefrontal cortex: structural re-organization of microglia and the inhibitory effect of minocycline. Cereb. Cortex 2012, 23(8):1784-1797. 10.1093/cercor/bhs151.
30. Imai Y., Ibata I., Ito D., Ohsawa K., Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 1996, 224(3):855-862. 10.1006/bbrc.1996.1112.
31. Imai Y., Koshaka S. Intracellular signalling in M-CSF-induced microglia activation: role of Iba1. Glia 2002, 40:164-174. 10.1002/glia.10149.
32. Jantaratnotai N., Utaisincharoen P., Sanvarinda P., Thampithak A., Sanvarinda Y. Phytoestrogens mediated anti-inflammatory effect through suppression of IRF-1 and pSTAT1 expressions in lipopolysaccharide-activated microglia. Int. Immunopharmacol. 2013, 483-488. 10.1016/j.intimp.2013.07.013.
33. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiol. Microglia. Physiol. Rev. 2011, 91(2):461-553. 10.1152/physrev.00011.2010.
34. Kim S.R., Kim S.U., Oh U., Jin B.K. Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+-mediated mitochondrial damage and cytochrome c release. J. Immunol. 2006, 177(7):4322-4329.
35. Kloss C.U., Bohatschek M., Kreutzberg G.W., Raivich G. Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp. Neurol. 2001, 168(1):32-46. 10.1006/exnr.2000.7575.
36. Komatsu T., Chiba T., Yamaza H., Yamashita K., Shimada A., Hoshiyama Y., Shimokawa I. Manipulation of caloric content but not diet composition, attenuates the deficit in learning and memory of senescence-accelerated mouse strain P8. Exp. Gerontol. 2008, 43(4):339-346. 10.1016/j.exger.2008.01.008.
37. Kondo S., Kohsaka S., Okabe S. Long-term changes of spine dynamics and microglia after transient peripheral immune response triggered by LPS in vivo. Mol. Brain 2011, 4:27. 10.1186/1756-6606-4-27.
38. Konsman J.P., Parnet P., Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci. 2002, 25(3):154-159. 10.1016/S0166-2236(00)02088-9.
39. Koubova J., Guarente L. How does calorie restriction work?. Genes Dev. 2007, 17(3):313-321. 10.1101/gad.1052903.
40. Kuroi T., Shimizu T., Shibata M., Toriumi H., Funakubo M., Iwashita T., Suzuki N. Alterations in microglia and astrocytes in the trigeminal nucleus caudalis by repetitive TRPV1 stimulation on the trigeminal nociceptors. NeuroReport 2012, 23(9):560-565. 10.1097/WNR.0b013e3283546242.
41. Lafrance V., Inoue W., Kan B., Luheshi G.N. Leptin modulates cell morphology and cytokine release in microglia. Brain Behav. Immun. 2010, 24(3):358-365. 10.1016/j.bbi.2009.11.003.
42. Lee S., Kim Y., Li E., Park S. Ghrelin protects spinal cord motoneurons against chronic glutamate excitotoxicity by inhibiting microglial activation. Korean J. Physiol. Pharmacol. 2012, 16(1):43-48. 10.4196/kjpp.2012.16.1.43.
43. Levay E.A., Govic A., Penman J., Paolini A.G., Kent S. Effects of adult-onset calorie restriction on anxiety-like behavior in rats. Physiol. Behav. 2007, 92(5):889-896. 10.1016/j.physbeh.2007.06.018.
44. Levay E.A., Tammer A.H., Penman J., Kent S., Paolini A.G. Calorie restriction at increasing levels leads to augmented concentrations of corticosterone and decreasing concentrations of testosterone in rats. Nutr. Res. 2010, 30(5):366-373. 10.1016/j.nutres.2010.05.001.
45. Loncarevic-Vasiljkovic N., Pesic V., Todorovic S., Popic J., Smiljanic K., Milanovic D., Kanazir S. Caloric restriction suppresses microglial activation and prevents neuroapoptosis following cortical injury in rats. PLoS ONE 2012, 7(5):e37215. 10.1371/journal.pone.0037215.
46. Luheshi G.N., Gardner J.D., Rushforth D.A., Loudon A.S., Rothwell N.J. Leptin actions on food intake and body temperature are mediated by IL-1. Proc. Natl. Acad. Sci. USA 1999, 96(12):7047-7052. 10.1073/pnas.96.12.7047.
47. MacDonald L., Begg D., Weisinger R.S., Kent S. Calorie restricted rats do not increase metabolic rate post-LPS, but do seek out warmer ambient temperatures to behaviourally induce a fever. Physiol. Behav. 2012, 107(5):762-772. 10.1016/j.physbeh.2012.06.009.
48. MacDonald L., Radler M., Paolini A.G., Kent S. Calorie restriction attenuates LPS-induced sickness behavior and shifts hypothalamic signaling pathways to an anti-inflammatory bias. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301(1):R172-184. 10.1152/ajpregu.00057.2011.
49. Madore C., Joffre C., Delpech J.C., De Smedt-Peyrusse V., Aubert A., Coste L., Nadjar A. Early morphofunctional plasticity of microglia in response to acute lipopolysaccharide. Brain Behav. Immun. 2013, Epub ahead of print retrieved September 3. 10.1016/j.bbi.2013.08.008.
50. Maswood N., Young J., Tilmont E., Zhang Z., Gash D.M., Gerhardt G.A., Ingram D.K Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 2004, 101(52):18171-18176. 10.1073/pnas.0405831102.
51. Matsuzaki J., Kuwamura M., Yamaji R., Inui H., Nakano Y. Inflammatory responses to lipopolysaccharide are suppressed in 40% energy-restricted mice. Nutr. Immunol. 2001, 131(8):2139-2144.
52. Morgan T.E., Xie Z., Goldsmith S., Yoshida T., Lanzrein A.S., Stone D., Finch C.E. The mosaic of brain glial hyperactivity during normal ageing and its attenuation by food restriction. Neuroscience 1999, 89(3):687-699. 10.1016/S0306-4522(98)00334-0.
53. Morris G.P., Clark I.A., Zinn R., Vissel B. Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research. Neurobiol. Learn. Mem. 2013, 105:40-53. 10.1016/j.nlm.2013.07.002.
54. Morton G.J., Cummings D.E., Baskin D.G., Barsh G.S., Schwartz M.W. Central nervous system control of food intake and body weight. Nature 2006, 443(7109):289-295. 10.1038/nature05026.
55. Nadeau S., Rivest S. Endotoxemia prevents the cerebral inflammatory wave induced by intraparenchymal lipopolysaccharide injection: role of glucocorticoids and CD14. J. Immunol. 2002, 169(6):3370-3381.
56. Nakajima K., Tohyama Y., Kohsaka S., Kurihara T. Ceramide activates microglia to enhance the production/secretion of brain-derived neurotrophic factor (BDNF) without induction of deleterious factors in vitro. J. Neurochem. 2002, 80(4):697-705. 10.1046/j.0022-3042.2001.00752.x.
57. Nakamura K. Central circuitries for body temperature regulation and fever. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301(5):R1207-1228. 10.1152/ajpregu.00109.2011.
58. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308(5726):1314-1318. 10.1126/science.1110647.
59. Otero M., Lago R., Gomez R., Dieguez C., Lago F., Gomez-Reino J., Gualillo O. Towards a pro-inflammatory and immunomodulatory emerging role of leptin. Rheumatology 2006, 45(8):944-950. 10.1093/rheumatology/kel157.
60. Pallant J. SPSS Survival Manual: A Step by Step Guide to Data Analysis using SPSS 2005, Allen & Unwin, Crows Nest, NSW.
61. Park E.S., Kim S.R., Jin B.K. Transient receptor potential vanilloid subtype 1 contributes to mesencephalic dopaminergic neuronal survival by inhibiting microglia-originated oxidative stress. Brain Res. Bull. 2012, 89(3-4):92-96. 10.1016/j.brainresbull.2012.07.001.
62. Patel N.V., Finch C.E. The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiol. Aging 2002, 23(5):707-717. 10.1016/S0197-4580(02)00017-9.
63. Peruzzo B., Pastor F.E., Blazquez J.L., Schobitz K., Pelaez B., Amat P., Rodriguez E.M. A second look at the barriers of the medial basal hypothalamus. Exp. Brain Res. 2000, 132(1):10-26. 10.1007/s002219900289.
64. Petersen R.G. Design and Analysis of Experiments 1985, Marcel Dekker Inc., New York.
65. Pezeshki G., Pohl T., Schobitz B. Corticosterone controls interleukin-1 beta expression and sickness behavior in the rat. J. Neuroendocrinol. 1996, 8(2):129-135. 10.1111/j.1365-2826.1996.tb00833.x.
66. Piccio L., Stark J.L., Cross A.H. Chronic calorie restriction attenuates experimental autoimmune encephalomyelitis. J. Leukoc. Biol. 2008, 84(4):940-948. 10.1189/jlb.0208133.
67. Pinteaux E., Inoue W., Schmidt L., Molina-Holgado F., Rothwell N.J., Luheshi G.N. Leptin induces interleukin-1beta release from rat microglial cells through a caspase 1 independent mechanism. J. Neurochem. 2007, 102(3):826-833. 10.1111/j.1471-4159.2007.04559.x.
68. Ponomarev E.D., Maresz K., Tan Y., Dittel B.N. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J. Neurosci. 2007, 27(40):10714-10721. 10.1523/JNEUROSCI.1922-07.2007.
69. Raghavendra V., Tanga F.Y., DeLeo J.A. Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur. J. Neurosci. 2004, 20(2):467-473. 10.1111/j.1460-9568.2004.03514.x.
70. Roth J., Harre E.M., Rummel C., Gerstberger R., Hubschle T. Signaling the brain in systemic inflammation: role of sensory circumventricular organs. Front. Biosci. 2004, 9:290-300. 10.2741/1241.
71. Rothwell N.J., Stock M.J. Effect of chronic food restriction on energy balance, thermogenic capacity, and brown-adipose-tissue activity in the rat. Biosci. Rep. 1982, 2(8):543-549. 10.1007/BF01314214.
72. Sabatino F., Masoro E.J., McMahan C.A., Kuhn R.W. Assessment of the role of the glucocorticoid system in aging processes and in the action of food restriction. J. Gerontol. 1991, 46(5):B171-179. 10.1093/geronj/46.5.B171.
73. Sakurada S., Shido O., Sugimoto N., Hiratsuka Y., Yoda T., Kanosue K. Autonomic and behavioural thermoregulation in starved rats. J. Physiol. 2000, 526(2):417-424. 10.1111/j.1469-7793.2000.00417.x.
74. Shaver S.W., Pang J.J., Wainman D.S., Wall K.M., Gross P.M. Morphology and function of capillary networks in subregions of the rat tuber cinereum. Cell Tissue Res. 1992, 267(3):437-448. 10.1007/BF00319366.
75. Shen A., Zhou D., Shen Q., Liu H.O., Sun L., Liu Y., Cheng C. The expression of tumor necrosis factor-alpha (TNF-alpha) by the intrathecal injection of lipopolysaccharide in the rat spinal cord. Neurochem. Res. 2009, 34(2):333-341. 10.1007/s11064-008-9780-z.
76. Sierra A., Encinas J.M., Deudero J.J., Chancey J.H., Enikolopov G., Overstreet-Wadiche L.S., Maletic-Savatic M. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 2010, 7(4):483-495. 10.1016/j.stem.2010.08.014.
77. Sonti G., Ilyin S.E., Plata-Salamàn C.R. Neuropeptide Y blocks and reverses interleukin-1 beta-induced anorexia in rats. Peptides 1996, 17(3):517-520. 10.1016/0196-9781(96)00016-2.
78. Steiner J., Mawrin C., Ziegeler A., Bielau H., Ullrich O., Bernstein H.G., Bogerts B. Distribution of HLA-DR-positive microglia in schizophrenia reflects impaired cerebral lateralization. Acta Neuropathol. 2006, 112(3):305-316. 10.1007/s00401-006-0090-8.
79. Streit W.J., Walter S.A., Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 1999, 57(6):563-581. 10.1016/S0301-0082(98)00069-0.
80. Sugama S., Takenouchi T., Fujita M., Conti B., Hashimoto M. Differential microglial activation between acute stress and lipopolysaccharide treatment. J. Neuroimmunol. 2009, 207(1-2):24-31. 10.1016/j.jneuroim.2008.11.007.
81. Sugama S., Takenouchi T., Fujita M., Kitani H., Conti B., Hashimoto M. Corticosteroids limit microglial activation occurring during acute stress. Neuroscience 2012, 232:13-20. 10.1016/j.neuroscience.2012.12.012.
82. Sugama S., Takenouchi T., Fujita M., Kitani H., Hashimoto M. Cold stress induced morphological microglial activation and increased IL-1beta expression in astroglial cells in rat brain. J. Neuroimmunol. 2011, 233(1-2):29-36. 10.1016/j.jneuroim.2010.11.002.
83. Takahashi K., Rochford C.D., Neumann H. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J. Exp. Med. 2005, 201(4):647-657. 10.1084/jem.20041611.
84. Tu Y.F., Lu P.J., Huang C.C., Ho C.J., Chou Y.P. Moderate dietary restriction reduces p53-mediated neurovascular damage and microglia activation after hypoxic ischemia in neonatal brain. Stroke 2012, 43(2):491-498. 10.1161/STROKEAHA.111.629931.
85. Tynan R.J., Naicker S., Hinwood M., Nalivaiko E., Buller K.M., Pow D.V., Walker F.R. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav. Immun. 2010, 24(7):1058-1068. 10.1016/j.bbi.2010.02.001.
86. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009, 10(6):397-409. 10.1038/nrn2647.
87. U.S.Department of Agriculture and U.S.Department of Health and Human Services Dietary Guidelines for Americans 2010, U.S. Government Printing Office, Washington, DC. 7th ed.
88. Van Dam A.M., Bauer J., Tilders F.J., Berkenbosch F. Endotoxin-induced appearance of immunoreactive interleukin-1 beta in ramified microglia in rat brain: a light and electron microscopic study. Neuroscience 1995, 65(3):815-826.
89. Wake H., Moorhouse A.J., Jinno S., Kohsaka S., Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 2009, 29(13):3974-3980. 10.1523/JNEUROSCI.4363-08.2009.
90. Wake H., Moorhouse A.J., Miyamoto A., Nabekura J. Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci. 2013, 36(4):209-217. 10.1016/j.tins.2012.11.007.
91. Walford R.L., Mock D., Verdery R., MacCallum T. Calorie restriction in biosphere 2: alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. J. Gerontol. A Biol. Sci.Med. Sci. 2002, 57(6):B211-224. 10.1093/gerona/57.6.B211.
92. Waseem T., Duxbury M., Ito H., Ashley S.W., Robinson M.K. Exogenous ghrelin modulates release of pro-inflammatory and anti-inflammatory cytokines in LPS-stimulated macrophages through distinct signaling pathways. Surgery 2008, 143(3):334-342. 10.1016/j.surg.2007.09.039.
93. Weindruch R., Walford R.L. The Retardation Of Aging And Disease By Dietary Restriction 1988, Charles C. Thomas, Springfield, IL.
94. Wrona D. Neural-immune interactions: an integrative view of the bidirectional relationship between the brain and immune systems. J. Neuroimmunol. 2006, 172(1-2):38-58. 10.1016/j.jneuroim.2005.10.017.
95. Zhang X., Li L., McNaughton P.A. Proinflammatory mediators modulate the heat-activated ion channel TRPV1 via the scaffolding protein AKAP79/150. Neuron 2008, 59(3):450-461. 10.1016/j.neuron.2008.05.015.
96. Ziv Y., Ron N., Butovsky O., Landa G., Sudai E., Greenberg N., Schwartz M. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 2006, 9(2):268-275. 10.1038/nn1629.