Potent and multiple regulatory actions of microglial glucocorticoid receptors during CNS inflammation

Cell Death and Differentiation

Volumn 20, Issue 11, 2013, Pages 1546-1557

  Carrillo De Sauvage, M A ^a,b,c,d   Maatouk, L ^a,b,c   Arnoux, I ^b,e   Pasco, M ^a,b,c   Sanz Diez, A ^b,e   Delahaye, M ^a,b,c   Herrero, M T ^d   Newman, T A ^f   Calvo, C F ^g   Audinat, E ^b,e   Tronche, F ^a,b,c   Vyas, S ^a,b,c  

^a CNRS   (France)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF MURCIA   (Spain)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^g INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

glucocorticoid receptors; inflammation; LPS; microglia; neuron survival

Indexed keywords

GLUCOCORTICOID RECEPTOR; LIPOPOLYSACCHARIDE; MIFEPRISTONE; MINERALOCORTICOID RECEPTOR; OXYGEN RADICAL; POTASSIUM CHANNEL KV1.3; TOLL LIKE RECEPTOR 4;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MOTILITY; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MICROGLIA; MOUSE; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRESS;

MUS;

ANIMALS; CELL GROWTH PROCESSES; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, TRANSGENIC; MICROGLIA; NERVE DEGENERATION; NEURONS; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 84885426536     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.108     Document Type: Article

References (57)

1. Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 2009; 27: 119-145.
2. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007; 10: 1387-1394.
3. Glezer I, Simard AR, Rivest S. Neuroprotective role of the innate immune system by microglia. Neuroscience 2007; 147: 867-883.
4. Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol 2009; 9: 429-439.
5. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
6. Sternberg EM. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat Rev Immunol 2006; 6: 318-328.
7. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K. Steroid hormone receptor expression and function in microglia. Glia 2008; 56: 659-674.
8. Saijo K, Collier JG, Li AC, Katzenellenbogen JA, Glass CK. An ADIOL-ERbeta-CtBP transrepression pathway negatively regulates microglia-mediated inflammation. Cell 2011; 145: 584-595.
9. Ros-Bernal F, Hunot S, Herrero MT, Parnadeau S, Corvol JC, Lu L et al. Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proc Natl Acad Sci USA 2011; 108: 6632-6637.
10. Fuller PJ, Yao Y, Yang J, Young MJ. Mechanisms of ligand specificity of the mineralocorticoid receptor. J Endocrinol 2012; 213: 15-24.
11. Usher MG, Duan SZ, Ivaschenko CY, Frieler RA, Berger S, Schutz G et al. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest 2010; 120: 3350-3364.
12. Frieler RA, Meng H, Duan SZ, Berger S, Schutz G, He Y et al. Myeloid-specific deletion of the mineralocorticoid receptor reduces infarct volume and alters inflammation during cerebral ischemia. Stroke 2011; 42: 179-185.
13. Goulding NJ. The molecular complexity of glucocorticoid actions in inflammation-a four-ring circus. Curr Opin Pharmacol 2004; 4: 629-636.
14. Nadeau S, Rivest S. Glucocorticoids play a fundamental role in protecting the brain during innate immune response. J Neurosci 2003; 23: 5536-5544.
15. Sugo N, Hurn PD, Morahan MB, Hattori K, Traystman RJ, DeVries AC. Social stress exacerbates focal cerebral ischemia in mice. Stroke 2002; 33: 1660-1664.
16. de Pablos RM, Villaran RF, Arguelles S, Herrera AJ, Venero JL, Ayala A et al. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci 2006; 26: 5709-5719.
17. Alexander JK, DeVries AC, Kigerl KA, Dahlman JM, Popovich PG. Stress exacerbates neuropathic pain via glucocorticoid and NMDA receptor activation. Brain Behav Immun 2009; 23: 851-860.
18. Munhoz CD, Lepsch LB, Kawamoto EM, Malta MB, Lima Lde S, Avellar MC et al. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neurosci 2006; 26: 3813-3820.
19. Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM, Bailey MT et al. beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci 2011; 31: 6277-6288.
20. Frank MG, Thompson BM, Watkins LR, Maier SF. Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav Immun 2012; 26: 337-345.
21. Njie EG, Boelen E, Stassen FR, Steinbusch HW, Borchelt DR, Streit WJ. Ex vivo cultures of microglia from young and aged rodent brain reveal age-related changes in microglial function. Neurobiol Aging 2012; 33: 195 e191-112.
22. Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR et al. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol 2009; 30: 325-333.
23. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011; 91: 461-553.
24. Boucsein C, Kettenmann H, Nolte C. Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur J Neurosci 2000; 12: 2049-2058.
25. Menteyne A, Levavasseur F, Audinat E, Avignone E. Predominant functional expression of Kv1.3 by activated microglia of the hippocampus after status epilepticus. PLoS One 2009; 4: e6770.
26. Fordyce CB, Jagasia R, Zhu X, Schlichter LC. Microglia Kv1.3 channels contribute to their ability to kill neurons. J Neurosci 2005; 25: 7139-7149.
27. Di Virgilio F, Ceruti S, Bramanti P, Abbracchio MP. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci 2009; 32: 79-87.
28. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I et al. Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 2009; 182: 7603-7612.
29. Burnstock G, Krugel U, Abbracchio MP, Illes P. Purinergic signalling: from normal behaviour to pathological brain function. Prog Neurobiol 2011; 95: 229-274.
30. Gessi S, Merighi S, Varani K, Borea PA. Adenosine receptors in health and disease. Adv Pharmacol 2011; 61: 41-75.
31. Jeong YH, Park CH, Yoo J, Shin KY, Ahn SM, Kim HS et al. Chronic stress accelerates learning and memory impairments and increases amyloid deposition in APPV717I-CT100 transgenic mice, an Alzheimer's disease model. FASEB J 2006; 20: 729-731.
32. Moreno B, Jukes JP, Vergara-Irigaray N, Errea O, Villoslada P, Perry VH et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol 2011; 70: 932-942.
33. Aguilera G. HPA axis responsiveness to stress: implications for healthy aging. Exp Gerontol 2011; 46: 90-95.
34. Jurgens HA, Johnson RW. Dysregulated neuronal-microglial cross-talk during aging, stress and inflammation. Exp Neurol 2012; 233: 40-48.
35. Johnson EA, O'Callaghan JP, Miller DB. Chronic treatment with supraphysiological levels of corticosterone enhances D-MDMA-induced dopaminergic neurotoxicity in the C57BL/6J female mouse. Brain Res 2002; 933: 130-138.
36. Rangon CM, Fortes S, Lelievre V, Leroux P, Plaisant F, Joubert C et al. Chronic mild stress during gestation worsens neonatal brain lesions in mice. J Neurosci 2007; 27: 7532-7540.
37. Frank MG, Miguel ZD, Watkins LR, Maier SF. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav Immun 2010; 24: 19-30.
38. Chakravarty S, Herkenham M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 2005; 25: 1788-1796.
39. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 2012; 109: E197-E205.
40. Lawson LJ, Perry VH, Dri P, Gordon S. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990; 39: 151-170.
41. Bousquet E, Zhao M, Ly A, Leroux Les Jardins G, Goldenberg B, Naud MC et al. The aldosterone-mineralocorticoid receptor pathway exerts anti-inflammatory effects in endotoxin-induced uveitis. PLoS One 7: e49036.
42. Holm TH, Draeby D, Owens T. Microglia are required for astroglial Toll-like receptor 4 response and for optimal TLR2 and TLR3 response. Glia 2012; 60: 630-638.
43. Xu L, Xu Z, Xu M. Glucocorticoid treatment restores the impaired suppressive function of regulatory T cells in patients with relapsing-remitting multiple sclerosis. Clin Exp Immunol 2009; 158: 26-30.
44. Chao CC, Hu S, Sheng WS, Tsang M, Peterson PK. Tumor necrosis factor-alpha mediates the release of bioactive transforming growth factor-beta in murine microglial cell cultures. Clin Immunol Immunopathol 1995; 77: 358-365.
45. Streit WJ, Walter SA, Pennell NA. Reactive microgliosis. Prog Neurobiol 1999; 57: 563-581.
46. Vitkovic L, Bockaert J, Jacque C. 'Inflammatory' cytokines: neuromodulators in normal brain? J Neurochem 2000; 74: 457-471.
47. Garden GA, Moller T. Microglia biology in health and disease. J Neuroimmune Pharmacol 2006; 1: 127-137.
48. Simard AR, Rivest S. Neuroprotective effects of resident microglia following acute brain injury. J Comp Neurol 2007; 504: 716-729.
49. Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 2007; 21: 47-59.
50. Sugama S, Fujita M, Hashimoto M, Conti B. Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 2007; 146: 1388-1399.
51. Espinosa-Oliva AM, de Pablos RM, Villaran RF, Arguelles S, Venero JL, Machado A et al. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging 2009; 32: 85-102.
52. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 1999; 23: 99-103.
53. Tuckermann JP, Kleiman A, Moriggl R, Spanbroek R, Neumann A, Illing A et al. Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. J Clin Invest 2007; 117: 1381-1390.
54. Schmued LC, Albertson C, Slikker W Jr. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res 1997; 751: 37-46.
55. Kawano T, Kunz A, Abe T, Girouard H, Anrather J, Zhou P et al. iNOS-derived NO and nox2-derived superoxide confer tolerance to excitotoxic brain injury through peroxynitrite. J Cereb Blood Flow Metab 2007; 27: 1453-1462.
56. Capone C, Fabrizi C, Piovesan P, Principato MC, Marzorati P, Ghirardi O et al. 2-Aminotetraline derivative protects from ischemia/reperfusion brain injury with a broad therapeutic window. Neuropsychopharmacology 2007; 32: 1302-1311.
57. Meme W, Calvo CF, Froger N, Ezan P, Amigou E, Koulakoff A et al. Proinflammatory cytokines released from microglia inhibit gap junctions in astrocytes: potentiation by beta-amyloid. FASEB J 2006; 20: 494-496.