Effect of stress and peripheral immune activation on astrocyte activation in transgenic bioluminescent Gfap-luc mice

GLIA

Volumn 63, Issue 7, 2015, Pages 1126-1137

  Biesmans, Steven ^a,b   Acton, Paul D ^b   Cotto, Carlos ^b   Langlois, Xavier ^a   Ver Donck, Luc ^a   Bouwknecht, Jan A ^a   Aelvoet, Sarah Ann ^c   Hellings, Niels ^b   Meert, Theo F ^a,b   Nuydens, Rony ^b  

^a HASSELT UNIVERSITY   (Belgium)

^b JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

^c KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Bioluminescence; Gfap luc mouse; Glial activation; Immune to brain; TSPO PET

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; LUCIFERASE; POLYINOSINIC POLYCYTIDYLIC ACID; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; NERVE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BIOLUMINESCENCE; CELL ACTIVATION; IN VIVO STUDY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; STRESS; TRANSGENIC MOUSE; ANIMAL; BRAIN; DISEASE MODEL; EXERCISE; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; LUMINESCENCE; MALE; MENTAL STRESS; METABOLISM; MICROGLIA; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION;

ANIMALS; ASTROCYTES; BRAIN; DISEASE MODELS, ANIMAL; INFLAMMATION; LIPOPOLYSACCHARIDES; LUCIFERASES; LUMINESCENT MEASUREMENTS; MALE; MICE, TRANSGENIC; MICROGLIA; NERVE TISSUE PROTEINS; NEUROIMMUNOMODULATION; POLY I-C; RANDOM ALLOCATION; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL;

EID: 84928214796     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22804     Document Type: Article

References (90)

1. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
2. Andre C, O'Connor JC, Kelley KW, Lestage J, Dantzer R, Castanon N. 2008. Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2, 3-dioxygenase in response to peripheral lipopolysaccharide administration. J Neuroimmunol 200:90-99.
3. Anisman H. 2009. Cascading effects of stressors and inflammatory immune system activation: Implications for major depressive disorder. J Psychiatry Neurosci 34:4-20.
4. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. 2010. Glial and neuronal control of brain blood flow. Nature 468:232-243.
5. Audet MC, Jacobson-Pick S, Wann BP, Anisman H. 2011. Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav Immun 25:1197-1205.
6. Barnum CJ, Pace TW, Hu F, Neigh GN, Tansey MG. 2012. Psychological stress in adolescent and adult mice increases neuroinflammation and attenuates the response to LPS challenge. J Neuroinflammation 9:9.
7. Beurel E. 2011. HDAC6 regulates LPS-tolerance in astrocytes. PLoS One 6:e25804.
8. Beurel E, Jope RS. 2010. Glycogen synthase kinase-3 regulates inflammatory tolerance in astrocytes. Neuroscience 169:1063-1070.
9. Biesmans S, Meert TF, Bouwknecht JA, Acton PD, Davoodi N, De HP, Kuijlaars J, Langlois X, Matthews LJ, Ver Donck L, Hellings N, Nuydens R. 2013. Systemic immune activation leads to neuroinflammation and sickness behavior in mice. Mediators Inflamm 2013:271359.
10. Borges BC, Rorato R, ntunes-Rodrigues J, Elias LL. 2012. Glial cell activity is maintained during prolonged inflammatory challenge in rats. Braz J Med Biol Res 45:784-791.
11. Bowers SL, Bilbo SD, Dhabhar FS, Nelson RJ. 2008. Stressor-specific alterations in corticosterone and immune responses in mice. Brain Behav Immun 22:105-113.
12. Briard E, Zoghbi SS, Simeon FG, Imaizumi M, Gourley JP, Shetty HU, Lu S, Fujita M, Innis RB, Pike VW. 2009. Single-step high-yield radiosynthesis and evaluation of a sensitive 18F-labeled ligand for imaging brain peripheral benzodiazepine receptors with PET. J Med Chem 52:688-699.
13. Broad A, Jones DE, Kirby JA. 2006. Toll-like receptor (TLR) response tolerance: A key physiological "damage limitation" effect and an important potential opportunity for therapy. Curr Med Chem 13:2487-2502.
14. Capoccia S, Berry A, Bellisario V, Vacirca D, Ortona E, Alleva E, Cirulli F. 2013. Quality and timing of stressors differentially impact on brain plasticity and neuroendocrine-immune function in mice. Neural Plast 2013:971817.
15. Casellas P, Galiegue S, Basile AS. 2002. Peripheral benzodiazepine receptors and mitochondrial function. Neurochem Int 40:475-486.
16. Castanon N, Medina C, Mormede C, Dantzer R. 2004. Chronic administration of tianeptine balances lipopolysaccharide-induced expression of cytokines in the spleen and hypothalamus of rats. Psychoneuroendocrinology 29:778-790.
17. Chen MK, Guilarte TR. 2008. Translocator protein 18 kDa (TSPO): Molecular sensor of brain injury and repair. Pharmacol Ther 118:1-17.
18. Ching AS, Kuhnast B, Damont A, Roeda D, Tavitian B, Dolle F. 2012. Current paradigm of the 18-kDa translocator protein (TSPO) as a molecular target for PET imaging in neuroinflammation and neurodegenerative diseases. Insights Imaging 3:111-119.
19. Connor TJ, Brewer C, Kelly JP, Harkin A. 2005. Acute stress suppresses pro-inflammatory cytokines TNF-alpha and IL-1 beta independent of a catecholamine-driven increase in IL-10 production. J Neuroimmunol 159:119-128.
20. Corcia P, Tauber C, Vercoullie J, Arlicot N, Prunier C, Praline J, Nicolas G, Venel Y, Hommet C, Baulieu JL, Cottier JP, Roussel C, Kassiou M, Guilloteau D, Ribeiro MJ. 2012. Molecular imaging of microglial activation in amyotrophic lateral sclerosis. PLoS One 7:e52941.
21. Cunningham C, Campion S, Teeling J, Felton L, Perry VH. 2007. The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain Behav Immun 21:490-502.
22. Curtin NM, Mills KH, Connor TJ. 2009. Psychological stress increases expression of IL-10 and its homolog IL-19 via beta-adrenoceptor activation: Reversal by the anxiolytic chlordiazepoxide. Brain Behav Immun 23:371-379.
23. De KJ, Mostert JP, Koch MW. 2008. Dysfunctional astrocytes as key players in the pathogenesis of central nervous system disorders. J Neurol Sci 267:3-16.
24. de Pablos RM, Villaran RF, Arguelles S, Herrera AJ, Venero JL, Ayala A, Cano J, Machado A. 2006. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci 26:5709-5719.
25. den Haan JM, Kraal G. 2012. Innate immune functions of macrophage subpopulations in the spleen. J Innate Immun 4:437-445.
26. Dhabhar FS. 2000. Acute stress enhances while chronic stress suppresses skin immunity. The role of stress hormones and leukocyte trafficking. Ann N Y Acad Sci 917:876-893.
27. Dhabhar FS. 2002. Stress-induced augmentation of immune function-The role of stress hormones, leukocyte trafficking, and cytokines. Brain Behav Immun 16:785-798.
28. Dhabhar FS, McEwen BS. 1997. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: A potential role for leukocyte trafficking. Brain Behav Immun 11:286-306.
29. Dickens AM, Vainio S, Marjamaki P, Johansson J, Lehtiniemi P, Rokka J, Rinne J, Solin O, Haaparanta-Solin M, Jones PA, Trigg W, Anthony DC, Airas L. 2014. Detection of microglial activation in an acute model of neuroinflammation using PET and radiotracers 11C-(R)-PK11195 and 18F-GE-180. J Nucl Med 55:466-472.
30. Dong Y, Benveniste EN. 2001. Immune function of astrocytes. Glia 36:180-190.
31. Erickson MA, Banks WA. 2011. Cytokine and chemokine responses in serum and brain after single and repeated injections of lipopolysaccharide: Multiplex quantification with path analysis. Brain Behav Immun 25:1637-1648.
32. Evans MS, Chaurette JP, Adams ST Jr, Reddy GR, Paley MA, Aronin N, Prescher JA, Miller SC. 2014. A synthetic luciferin improves bioluminescence imaging in live mice. Nat Methods 11:393-395.
33. Farina C, Aloisi F, Meinl E. 2007. Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138-145.
34. Foster SL, Medzhitov R. 2009. Gene-specific control of the TLR-induced inflammatory response. Clin Immunol 130:7-15.
35. Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF. 2007. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 21:47-59.
36. Gibney SM, McGuinness B, Prendergast C, Harkin A, Connor TJ. 2013. Poly I:C-induced activation of the immune response is accompanied by depression and anxiety-like behaviours, kynurenine pathway activation and reduced BDNF expression. Brain Behav Immun 28:170-181.
37. Glaser R, Kiecolt-Glaser JK. 2005. Stress-induced immune dysfunction: Implications for health. Nat Rev Immunol 5:243-251.
38. Godbout JP, Glaser R. 2006. Stress-induced immune dysregulation: Implications for wound healing, infectious disease and cancer. J Neuroimmune Pharmacol 1:421-427.
39. Goujon E, Parnet P, Laye S, Combe C, Kelley KW, Dantzer R. 1995. Stress downregulates lipopolysaccharide-induced expression of proinflammatory cytokines in the spleen, pituitary, and brain of mice. Brain Behav Immun 9:292-303.
40. Grippo AJ, Francis J, Beltz TG, Felder RB, Johnson AK. 2005. Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol Behav 84:697-706.
41. Gulyas B, Toth M, Schain M, Airaksinen A, Vas A, Kostulas K, Lindstrom P, Hillert J, Halldin C. 2012. Evolution of microglial activation in ischaemic core and peri-infarct regions after stroke: A PET study with the TSPO molecular imaging biomarker [((11))C]vinpocetine. J Neurol Sci 320:110-117.
42. Hamby ME, Sofroniew MV. 2010. Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7:494-506.
43. Hannestad J, Gallezot JD, Schafbauer T, Lim K, Kloczynski T, Morris ED, Carson RE, Ding YS, Cosgrove K. 2012. Endotoxin-induced systemic inflammation activates microglia: [(11)C]PBR28 positron emission tomography in nonhuman primates. Neuroimage 63:232-239.
44. Hardwick MJ, Chen MK, Baidoo K, Pomper MG, Guilarte TR. 2005. In vivo imaging of peripheral benzodiazepine receptors in mouse lungs: A biomarker of inflammation. Mol Imaging 4:432-438.
45. Hatori A, Yui J, Yamasaki T, Xie L, Kumata K, Fujinaga M, Yoshida Y, Ogawa M, Nengaki N, Kawamura K, Fukumura T, Zhang MR. 2012. PET imaging of lung inflammation with [18F]FEDAC, a radioligand for translocator protein (18 kDa). PLoS One 7:e45065.
46. Imaizumi M, Briard E, Zoghbi SS, Gourley JP, Hong J, Fujimura Y, Pike VW, Innis RB, Fujita M. 2008. Brain and whole-body imaging in nonhuman primates of [11C]PBR28, a promising PET radioligand for peripheral benzodiazepine receptors. Neuroimage 39:1289-1298.
47. Imbe H, Kimura A, Donishi T, Kaneoke Y. 2012. Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter. Neuroscience 223:209-218.
48. Imbe H, Kimura A, Donishi T, Kaneoke Y. 2013. Effects of restraint stress on glial activity in the rostral ventromedial medulla. Neuroscience 241:10-21.
49. Jany PL, Hagemann TL, Messing A. 2013. GFAP expression as an indicator of disease severity in mouse models of Alexander disease. ASN Neuro 5:81-88.
50. Jones HA, Marino PS, Shakur BH, Morrell NW. 2003. In vivo assessment of lung inflammatory cell activity in patients with COPD and asthma. Eur Respir J 21:567-573.
51. Jones HA, Valind SO, Clark IC, Bolden GE, Krausz T, Schofield JB, Boobis AR, Haslett C. 2002. Kinetics of lung macrophages monitored in vivo following particulate challenge in rabbits. Toxicol Appl Pharmacol 183:46-54.
52. Kaissling B, Hegyi I, Loffing J, Le HM. 1996. Morphology of interstitial cells in the healthy kidney. Anat Embryol (Berl) 193:303-318.
53. Kipp M, Norkute A, Johann S, Lorenz L, Braun A, Hieble A, Gingele S, Pott F, Richter J, Beyer C. 2008. Brain-region-specific astroglial responses in vitro after LPS exposure. J Mol Neurosci 35:235-243.
54. Kondo S, Kohsaka S, Okabe S. 2011. Long-term changes of spine dynamics and microglia after transient peripheral immune response triggered by LPS in vivo. Mol Brain 4:27.
55. Kuhlmann AC, Guilarte TR. 2000. Cellular and subcellular localization of peripheral benzodiazepine receptors after trimethyltin neurotoxicity. J Neurochem 74:1694-1704.
56. Kuo C, Coquoz O, Troy TL, Xu H, Rice BW. 2007. Three-dimensional reconstruction of in vivo bioluminescent sources based on multispectral imaging. J Biomed Opt 12:024007.
57. Kwon MS, Seo YJ, Lee JK, Lee HK, Jung JS, Jang JE, Park SH, Suh HW. 2008. The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci Lett 430:258-263.
58. Lai AY, Dhami KS, Dibal CD, Todd KG. 2011. Neonatal rat microglia derived from different brain regions have distinct activation responses. Neuron Glia Biol 7:5-16.
59. Lavisse S, Guillermier M, Herard AS, Petit F, Delahaye M, Van Camp N, Ben HL, Lebon V, Remy P, Dolle F, Delzescaux T, Bonvento G, Hantraye P, Escartin C. 2012. Reactive astrocytes overexpress TSPO and are detected by TSPO positron emission tomography imaging. J Neurosci 32:10809-10818.
60. Meltzer JC, MacNeil BJ, Sanders V, Pylypas S, Jansen AH, Greenberg AH, Nance DM. 2004. Stress-induced suppression of in vivo splenic cytokine production in the rat by neural and hormonal mechanisms. Brain Behav Immun 18:262-273.
61. Nair A, Bonneau RH. 2006. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 171:72-85.
62. Nguyen KT, Deak T, Owens SM, Kohno T, Fleshner M, Watkins LR, Maier SF. 1998. Exposure to acute stress induces brain interleukin-1beta protein in the rat. J Neurosci 18:2239-2246.
63. Nguyen KT, Deak T, Will MJ, Hansen MK, Hunsaker BN, Fleshner M, Watkins LR, Maier SF. 2000. Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Res 859:193-201.
64. O'Connor KA, Johnson JD, Hansen MK, Wieseler Frank JL, Maksimova E, Watkins LR, Maier SF. 2003. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 991:123-132.
65. Olsen AL, Morrey JD, Smee DF, Sidwell RW. 2007. Correlation between breakdown of the blood-brain barrier and disease outcome of viral encephalitis in mice. Antiviral Res 75:104-112.
66. Padgett DA, Marucha PT, Sheridan JF. 1998. Restraint stress slows cutaneous wound healing in mice. Brain Behav Immun 12:64-73.
67. Painsipp E, Kofer MJ, Sinner F, Holzer P. 2011. Prolonged depression-like behavior caused by immune challenge: Influence of mouse strain and social environment. PLoS One 6:e20719.
68. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A. 2012. Glial cells in (patho)physiology. J Neurochem 121:4-27.
69. Persoons JH, Berkenbosch F, Schornagel K, Thepen T, Kraal G. 1995. Increased specific IgE production in lungs after the induction of acute stress in rats. J Allergy Clin Immunol 95:765-770.
70. Puentener U, Booth SG, Perry VH, Teeling JL. 2012. Long-term impact of systemic bacterial infection on the cerebral vasculature and microglia. J Neuroinflammation 9:146.
71. Quan N, Avitsur R, Stark JL, He L, Shah M, Caligiuri M, Padgett DA, Marucha PT, Sheridan JF. 2001. Social stress increases the susceptibility to endotoxic shock. J Neuroimmunol 115:36-45.
72. Raya-Callis C, Hiemke C, Abumaria N, Flugge G. 2012. Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus. Psychopharmacology (Berl) 224:209-222.
73. Ridet JL, Malhotra SK, Privat A, Gage FH. 1997. Reactive astrocytes: Cellular and molecular cues to biological function. Trends Neurosci 20:570-577.
74. Skelly DT, Hennessy E, Dansereau MA, Cunningham C. 2013. A systematic analysis of the peripheral and CNS effects of systemic LPS, IL-1Beta, TNF-alpha and IL-6 challenges in C57BL/6 mice. PLoS One 8:e69123.
75. Sofroniew MV. 2005. Reactive astrocytes in neural repair and protection. Neuroscientist 11:400-407.
76. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
77. Sofroniew MV, Vinters HV. 2010. Astrocytes: Biology and pathology. Acta Neuropathol 119:7-35.
78. Sugama S, Fujita M, Hashimoto M, Conti B. 2007. Stress induced morphological microglial activation in the rodent brain: Involvement of interleukin-18. Neuroscience 146:1388-1399.
79. Takano T, Tian GF, Peng W, Lou N, Libionka W, Han X, Nedergaard M. 2006. Astrocyte-mediated control of cerebral blood flow. Nat Neurosci 9:260-267.
80. Tynan RJ, Beynon SB, Hinwood M, Johnson SJ, Nilsson M, Woods JJ, Walker FR. 2013. Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol 126:75-91.
81. Vasey MW, Thayer JF. 1987. The continuing problem of false positives in repeated measures ANOVA in psychophysiology: A multivariate solution. Psychophysiology 24:479-486.
82. Venneti S, Wang G, Nguyen J, Wiley CA. 2008. The positron emission tomography ligand DAA1106 binds with high affinity to activated microglia in human neurological disorders. J Neuropathol Exp Neurol 67:1001-1010.
83. Viswanathan K, Dhabhar FS. 2005. Stress-induced enhancement of leukocyte trafficking into sites of surgery or immune activation. Proc Natl Acad Sci USA 102:5808-5813.
84. Volterra A, Meldolesi J. 2005. Astrocytes, from brain glue to communication elements: The revolution continues. Nat Rev Neurosci 6:626-640.
85. Weber MD, Frank MG, Sobesky JL, Watkins LR, Maier SF. 2013. Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain Behav Immun 32:112-121.
86. Wohleb ES, Fenn AM, Pacenta AM, Powell ND, Sheridan JF, Godbout JP. 2012. Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice. Psychoneuroendocrinology 37:1491-1505.
87. Yasuno F, Kosaka J, Ota M, Higuchi M, Ito H, Fujimura Y, Nozaki S, Takahashi S, Mizukami K, Asada T, Suhara T. 2012. Increased binding of peripheral benzodiazepine receptor in mild cognitive impairment-dementia converters measured by positron emission tomography with [(1)(1)C]DAA1106. Psychiatry Res 203:67-74.
88. Zhang Y, Foster R, Sun X, Yin Q, Li Y, Hanley G, Stuart C, Gan Y, Li C, Zhang Z, Yin D. 2008a. Restraint stress induces lymphocyte reduction through p53 and PI3K/NF-kappaB pathways. J Neuroimmunol 200:71-76.
89. Zhang Y, Woodruff M, Zhang Y, Miao J, Hanley G, Stuart C, Zeng X, Prabhakar S, Moorman J, Zhao B, Yin D. 2008b. Toll-like receptor 4 mediates chronic restraint stress-induced immune suppression. J Neuroimmunol 194:115-122.
90. Zhu L, Ramboz S, Hewitt D, Boring L, Grass DS, Purchio AF. 2004. Non-invasive imaging of GFAP expression after neuronal damage in mice. Neurosci Lett 367:210-212.