Immune activation promotes depression 1 month after diffuse brain injury: A role for primed microglia

Biological Psychiatry

Volumn 76, Issue 7, 2014, Pages 575-584

  Fenn, Ashley M ^a   Gensel, John C ^b   Huang, Yan ^a   Popovich, Phillip G ^a   Lifshitz, Jonathan ^c   Godbout, Jonathan P ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Cytokines; Depression; Fluid percussion injury; Lipopolysaccharide; Major histocompatibility complex II; Microglia

Indexed keywords

INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEPRESSION; DISEASE COURSE; IMMOBILITY; IMMUNOSTIMULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICROGLIA; MOTOR COORDINATION; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; ROTAROD TEST; TAIL SUSPENSION TEST; TRAUMATIC BRAIN INJURY; ANIMAL; BAGG ALBINO MOUSE; BRAIN INJURY; COMPLICATION; ENCEPHALITIS; GLIOSIS; IMMUNOLOGY; METABOLISM; MOTOR ACTIVITY; TIME;

ANIMALS; BRAIN INJURIES; DEPRESSION; ENCEPHALITIS; GLIOSIS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MICROGLIA; MOTOR ACTIVITY; TIME FACTORS;

EID: 84922638429     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.10.014     Document Type: Article

References (75)

1. McCrea M, Guskiewicz KM, Marshall SW, Barr W, Randolph C, Cantu RC, et al. (2003): Acute effects and recovery time following concussion in collegiate football players: The NCAA concussion study. JAMA 290: 2556-2563.
2. Lifshitz J, Witgen B, Grady M (2007): Acute cognitive impairment after lateral fluid percussion brain injury recovers by 1 month: Evaluation by conditioned fear response. Behav Brain Res 177:347-357.
3. Tang Y, Noda Y, Hasegawa T, Nabeshima T (1997): A concussive-like brain injury model in mice (I): Impairment in learning and memory. J Neurotrauma 14:851-862.
4. Woodcock T, Morganti-Kossmann MC (2013): The role of markers of inflammation in traumatic brain injury. Front Neurol 4:18.
5. Jorge R, Robinson R, Arndt S, Starkstein S, Forrester A, Geisler F (1993): Depression following traumatic brain injury: A 1 year longitudinal study. J Affect Disorders 27:233-243.
6. Fleminger S (2008): Long-term psychiatric disorders after traumatic brain injury. Eur J Anesth 25:123-130.
7. Kreutzer JS, Seel RT, Gourley E (2001): The prevalence and symptom rates of depression after traumatic brain injury: A comprehensive examination. Brain Injury 15:563-576.
8. Gualtieri T, Cox DR (1991): The delayed neurobehavioural sequelae of traumatic brain injury. Brain Injury 5:219-232.
9. Jorge R, Robinson R, Moser D, Tateno A, Crespo-Facorro B, Arndt S (2004): Major depression following traumatic brain injury. Arch Gen Psychiatry 61:42-50.
10. Hibbard MR, Uysal S, Kepler K, Bogdany J, Silver J (1998): Axis I psychopathology in individuals with traumatic brain injury. J Head Trauma Rehab 13:24-39.
11. Holsinger T, Steffens DC, Phillips C, Helms MJ, Havlik RJ, Breitner JC, et al. (2002): Head injury in early adulthood and the lifetime risk of depression. Arch Gen Psychiatry 59:17-22.
12. Teasdale T, Engberg A (2001): Suicide after traumatic brain injury: A population study. J Neurol Neurosurg Psychiatry 71:436-440.
13. Saran A (1988): Antidepressants not effective in headache associated with minor closed head injury. Int J Psychiat Med 18:75-83.
14. Ashman TA, Cantor JB, Gordon WA, Spielman L, Flanagan S, Ginsberg A, et al. (2009): A randomized controlled trial of sertraline for the treatment of depression in persons with traumatic brain injury. Arch Phys Med Rehab 90:733-740.
15. Miller AH, Raison CL (2008): Immune system contributions to the pathophysiology of depression. Focus 6:36-45.
16. Raison CL, Capuron L, Miller AH (2006): Cytokines sing the blues: Inflammation and the pathogenesis of depression. Trends Immunol 27: 24-31.
17. Lanquillon S, Krieg JC, Bening-Abu-Shach U, Vedder H (2000): Cytokine production and treatment response in major depressive disorder. Neuropsychopharmacology 22:370-379.
18. Maier B, Schwerdtfeger K, Mautes A, Holanda M, Muller M, Steudel WI, et al. (2001): Differential release of interleukines 6, 8, and 10 in cerebrospinal fluid and plasma after traumatic brain injury. Shock 15: 421-426.
19. Fassbender K, Schneider S, Bertsch T, Schlueter D, Fatar M, Ragoschke A, et al. (2000): Temporal profile of release of interleukin-b in neurotrauma. Neurosci Lett 284:135.
20. Kossmann T, Hans VH, Imhof HG, Stocker R, Grob P, Trentz O, et al. (1995): Intrathecal and serum interleukin-6 and the acute-phase response in patients with severe traumatic brain injuries. Shock 4:311-317.
21. Gentleman SM, Leclercq PD, Moyes L, Graham DI, Smith C, Griffin WST, et al. (2004): Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int 146:97-104.
22. Barrientos R, Frank M, Watkins L, Maier S (2010): Memory impairments in healthy aging: Role of aging-induced microglial sensitization. Aging Dis 1:212-231.
23. Henry C, Huang Y, Wynne AM, Godbout JP (2009): Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both proinflammatory IL-1[beta] and anti-inflammatory IL-10 cytokines. Brain Behav Immun 23:309-317.
24. 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. Psychoneuroendocrinol 37:1491-1505.
25. Bland ST, Beckley JT, Young S, Tsang V, Watkins LR, Maier SF, et al. (2010): Enduring consequences of early-life infection on glial and neural cell genesis within cognitive regions of the brain. Brain Behav Immun 24:329-338.
26. Cunningham C, Campion S, Lunnon K, Murray CL, Woods JFC, Deacon RMJ, et al. (2009): Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol Psychiatry 65:304-312.
27. Palin K, Cunningham C, Forse P, Perry VH, Platt N (2008): Systemic inflammation switches the inflammatory cytokine profile in CNS wallerian degeneration. Neurobiol Dis 30:19-29.
28. Jurgens HA, Johnson RW (2012): Dysregulated neuronal-microglial cross-talk during aging, stress and inflammation. Exp Neurol 233:40-48.
29. Tremblay M-E, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A (2011): The role of microglia in the healthy brain. J Neurosci 31: 16064-16069.
30. Chen J, Buchanan J, Sparkman N, Godbout J, Freund G, Johnson R (2008): Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 22:301-311.
31. Barrientos RM, Frank MG, Hein AM, Higgins EA, Watkins LR, Rudy JW, et al. (2009): Time course of hippocampal IL-1 [beta] and memory consolidation impairments in aging rats following peripheral infection. Brain Behav Immun 23:46-54.
32. Godbout J, Chen J, Abraham J, Richwine A, Berg B, Kelley K, et al. (2005): Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 10:1329-1331.
33. Huang Y, Henry C, Dantzer R, Johnson R, Godbout J (2008): Exaggerated sickness behavior and brain proinflammatory cytokine expression in aged mice in response to intracerebroventricular lipopolysaccharide. Neurobiol Aging 29:1744-1753.
34. Godbout J, Moreau M, Lestage J, Chen J, Sparkman N, O'Connor J, et al. (2008): Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacol 33:2341-2351.
35. Holmin S, Mathiesen T, Shetye J, Biberfeld P (1995): Intracerebral inflammatory response to experimental brain contusion. Acta Nirochlrurglca 132:110-119.
36. Lifshitz J, Kelley BJ, Povlishock JT (2007): Perisomatic thalamic axotomy after diffuse traumatic brain injury is associated with atrophy rather than cell death. J Neuropathol Exp Neurol 66:218-229.
37. Morales D, Marklund N, Lebold D, Thompson H, Pitkanen A, Maxwell W, et al. (2005): Experimental models of traumatic brain injury: Do we really need to build a better mousetrap? Neuroscience 136:971-989.
38. Lifshitz J (2009): Fluid percussion injury model. In: Chen J, Xu ZC, Xu X-M, Zhang JH, editors. Animal Models of Acute Neurological Injuries. Clifton, NJ: Humana Press, 369-384.
39. Fenn AM, Henry CJ, Huang Y, Dugan A, Godbout JP (2012): 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 26:766-777.
40. Witgen B, Lifshitz J, Smith M, Schwarzbach E, Liang S, Grady M, et al. (2005): Regional hippocampal alteration associated with cognitive deficit following experimental brain injury: A systems, network and cellular evaluation. Neuroscience 133:1-15.
41. Bachstetter AD, Rowe RK, Kaneko M, Goulding D, Lifshitz J, Van Eldik LJ (2013): The p38[alpha] mapk regulates microglial responsiveness to diffuse traumatic brain injury. J Neurosci 33:6143-6153.
42. Kelley BJ, Lifshitz J, Povlishock JT (2007): Neuroinflammatory responses after experimental diffuse traumatic brain injury. J Neuropathol Exp Neurol 66:989-1001.
43. Kelley BJ, Farkas O, Lifshitz J, Povlishock JT (2006): Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Exp Neurol 198:350-360.
44. Witgen B, Lifshitz J, Grady M (2006): Inbred mouse strains as a tool to analyze hippocampal neuronal loss after brain injury: A stereological study. J Neurotraum 23:1320-1329.
45. Dunham N, Miya T (1957): A note on a simple apparatus for detecting neurological deficits in rats and mice. J Am Pharmacol Assoc 46: 208-209.
46. Corona A, Huang Y, O'Connor J, Dantzer R, Kelley K, Popovich P, et al. (2010): Fractalkine receptor (CS3CR1) deficiency sensitizes mice to the behavioral changes induced by lipopolysaccharide. J Neuroinflamm 7:93.
47. Corona AW, Norden DM, Skendelas JP, Huang Y, O'Connor JC, Lawson M, et al. (2013): Indoleamine 2, 3-dioxygenase inhibition attenuates lipopolysaccharide induced persistent microglial activation and depressive-like complications in fractalkine receptor (CX3CR1)-deficient mice. Brain Behav Immun 31:134-142.
48. Henry C, Huang Y, Wynne A, Hanke M, Himler J, Bailey M, et al. (2008): Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflamm 5:15.
49. Paxinos G, Franklin K (2004): The Mouse Brain in Stereotaxic Coordinates. 2nd ed. Waltham, MA: Academic Press Inc.
50. Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LTM, Bailey MT, et al. (2011): [beta]-adrenergic receptor antagonism prevents anxietylike behavior and microglial reactivity induced by repeated social defeat. J Neurosci 31:6277.
51. Donnelly DJ, Gensel JC, Ankeny DP, van Rooijen N, Popovich PG (2009): An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology. J Neurosci Meth 181:36-44.
52. Hamm RJ (2001): Neurobehavioral assessment of outcome following traumatic brain injury in rats: An evaluation of selected measures. J Neurotrauma 18:1207-1216.
53. McIntosh TK, Noble L, Andrews B, Faden AI (1987): Traumatic brain injury in the rat: Characterization of a midline fluid-percussion model. Cent Nerv Syst Trauma 4:119-134.
54. Schmidt RH, Grady MS (1993): Regional patterns of blood-brain barrier breakdown following central and lateral fluid percussion injury in rodents. J Neurotrauma 10:415-430.
55. El-Yacoubi M, Bouali S, Popa D, Naudon L, Leroux-Nicollet I, Hamon M, et al. (2003): Behavioral, neurochemical, and electrophysiological characterization of a genetic mouse model of depression. Proc Natl Acad Sci U S A 100:6227-6232.
56. Williamson LL, Sholar PW, Mistry RS, Smith SH, Bilbo SD (2011): Microglia and memory: Modulation by early-life infection. J Neurosci 31:15511-15521.
57. Bilbo SD, Schwarz JM (2009): Early-life programming of later-life brain and behavior: A critical role for the immune system. Front Behav Neurosci 3:14.
58. Murray C, Sanderson DJ, Barkus C, Deacon RMJ, Rawlins JNP, Bannerman DM, et al. (2010): Systemic inflammation induces acute working memory deficits in the primed brain: Relevance for delirium. Neurobiol Aging 33:603-616.
59. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH (2005): Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275-9284.
60. David S, Kroner A (2011): Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12:388-399.
61. Chen Z, Jalabi W, Shpargel KB, Farabaugh KT, Dutta R, Yin X, et al. (2012): Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. J Neurosci 32:11706-11715.
62. Frank M, Barrientos R, Biedenkapp J, Rudy J, Watkins L, Maier S (2006): mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging 27:717-722.
63. Streit WJ (2004): Microglia and Alzheimer's disease pathogenesis. J Neurosci Res 77:1-8.
64. Ramlackhansingh AF, Brooks DJ, Greenwood RJ, Bose SK, Turkheimer FE, Kinnunen KM, et al. (2011): Inflammation after trauma: Microglial activation and traumatic brain injury. Ann Neurol 70:374-383.
65. Ban E, Milon G, Prudhomme N, Fillion G, Haour F (1991): Receptors for interleukin-1 ([alpha] and [beta]) in mouse brain: Mapping and neuronal localization in hippocampus. Neuroscience 43:21-30.
66. Cunningham ET, Wada E, Carter DB, Tracey DE, Battey JF, De Souza EB (1992): In situ histochemical localization of type I interleukin-1 receptor messenger RNA in the central nervous system, pituitary, and adrenal gland of the mouse. J Neurosci 12:1101-1114.
67. Williamson LL, Bilbo SD (2013): Chemokines and the hippocampus: A new perspective on hippocampal plasticity and vulnerability. Brain Behav Immun 30:186-194.
68. Godbout JP, Johnson RW (2009): Age and neuroinflammation: A lifetime of psychoneuroimmune consequences. Immunol Allergy Clin 29:321-337.
69. Corona A, Fenn A, Godbout J (2012): Cognitive and behavioral consequences of impaired immunoregulation in aging. J Neuroimmune Pharm 7:7-23.
70. Beck A, Ward C, Mendelson M, Mock J, Erbaugh J (1961): An inventory for measuring depression. Arch Gen Psychiatry 4:561-571.
71. Maher FO, Nolan Y, Lynch MA (2005): Downregulation of IL-4-induced signalling in hippocampus contributes to deficits in LTP in the aged rat. Neurobiol Aging 26:717-728.
72. Dantzer R, O'Connor J, Freund G, Johnson R, Kelley K (2008): From inflammation to sickness and depression: When the immune system subjugates the brain. Nat Rev Neurosci 9:46-56.
73. Frenois F, Moreau M, O'Connor J, Lawson M, Micon C, Lestage J, et al. (2007): Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 32:516-531.
74. Steiner J, Walter M, Gos T, Guillemin G, Bernstein H-G, Sarnyai Z, et al. (2011): Severe depression is associated with increased microglial quinolinic acid in subregions of the anterior cingulate gyrus: Evidence for an immune-modulated glutamatergic neurotransmission? J Neuroinflamm 8:94.
75. Dantzer R, O'Connor JC, Lawson MA, Kelley KW (2011): Inflammationassociated depression: From serotonin to kynurenine. Psychoneuroendocrinology 36:426-436.