Spreading depression requires microglia and is decreased by their M2a polarization from environmental enrichment

GLIA

Volumn 62, Issue 7, 2014, Pages 1176-1194

  Pusic, Kae M ^a   Pusic, Aya D ^a   Kemme, Jordan ^a   Kraig, Richard P ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Environmental enrichment; Hippocampal slice culture; Interleukin 11; Microglial polarization; Migraine

Indexed keywords

CLODRONIC ACID; INTERLEUKIN 11; LIPOSOME; MENADIONE; MINOCYCLINE; TUMOR NECROSIS FACTOR ALPHA; CENTRAL NERVOUS SYSTEM AGENTS; CYTOKINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTROPHYSIOLOGY; ENVIRONMENTAL ENRICHMENT; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MICROGLIA; MICROGLIAL CELL CULTURE; MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN CONTENT; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SLICE CULTURE; SPREADING CORTICAL DEPRESSION; ANIMAL; ANIMAL HOUSING; CELL CULTURE; DRUG EFFECTS; ENVIRONMENT; MEMBRANE POTENTIAL; METABOLISM; MICROELECTRODE; NEOCORTEX; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE; WISTAR RAT;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM AGENTS; CYTOKINES; ENVIRONMENT; HIPPOCAMPUS; HOUSING, ANIMAL; INTERLEUKIN-11; MALE; MEMBRANE POTENTIALS; MICROELECTRODES; MICROGLIA; MINOCYCLINE; NEOCORTEX; OXIDATIVE STRESS; RATS, WISTAR; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900799748     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22672     Document Type: Article

References (88)

1. 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.
2. Brewer GJ, Torricelli JR, Evege EK, Price PJ. 1993. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
3. Bureš J, Burešová O, Křivánek J. 1974. The mechanism and applications of Leão's spreading depression of electroencelphalographic activity. Prague: Academia.
4. 2 and 4-Aminopyridine prevent the lipopolysaccharide-induced outwardly rectifying potassium current and interleukin-1β production in cultured rat microglia. J Neurochem 70:2357-2368.
5. Chen Y, Stevens B, Chang J, Milbrandt J, Barres BA, Hell JW. 2008. NS21: Re-defined and modified supplement B27 for neuronal cultures. J Neurosci Methods 171:239-247.
6. Chhor V, Le Charpentier T, Lebon S, Ore MV, Celador IL, Josserand J, Degos V, Jacotot E, Hagberg H, Savman K, Mallard C, Gressens P, Fleiss B. 2013. Characterization of phenotype markers and neuronotoxic potential of polarized primary microglia in vitro. Brain Behav Immun 32:70-85.
7. Cook D, Sanchez-Carbente Mdel R, Lachance C, Radzioch D, Tremblay S, Khandjian EW, Desgroseillers L, Murai KK. 2011. Fragile X related protein 1 clusters with ribosomes and messenger RNAs at a subset of dendritic spines in the mouse hippocampus. PLoS One 6:e26120.
8. Darabaneanu S, Overath CH, Rubin D, Luthje S, Sye W, Niederberger U, Gerber WD, Weisser B. 2011. Aerobic exercise as a therapy option for migraine: A pilot study. Int J Sports Med 32:455-460.
9. Devinsky O, Vezzani A, Najjar S, De Lanerolle NC, Rogawski MA. 2013. Glia and epilepsy: Excitability and inflammation. Trends in Neurosci 37:174-184.
10. Dreier JP, Major S, Pannek HW, Woitzik J, Scheel M, Wiesenthal D, Martus P, Winkler MKL, Hartings JA, Fabricius M, Speckmann EJ, Gorji A, COSBID study group. 2011. Spreading convulsions, spreading depolarizations and epileptogenesis in human cerebral cortex. Brain 135:259-275.
11. Dringen R. 2005. Oxidative and antioxidative potential of brain microglial cells. Antioxid Redox Signal 7:1223-1233.
12. Durafourt BA, Moore CS, Zammit DA, Johnson TA, Zaguia F, Guiot MC, Bar-Or A, Antel JP. 2012. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 60:717-727.
13. Eder C, Schilling T, Heinemann U, Haas D, Hailer N, Nitsch R. 1999. Morphological, immunophenotypical and electrophysiological properties of resting microglia in vitro. Eur J Neurosci 11:4251-4261.
14. Fares RP, Belmeguenai A, Sanchez PE, Kouchi HY, Bodennec J, Morales A, Georges B, Bonnet C, Bouvard S, Sloviter RS, Bezin L. 2013. Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats. PLoS One 8:e53888
15. Fabel K, Wolf SA, Ehninger D, Babu H, Leal-Galicia P, Kempermann G. 2009. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 3:50.
16. Frei K, Bodmer S, Schwerdel C, Fontana A. 1986. Astrocyte-derived interleukin 3 as a growth factor for microglia cells and peritoneal macrophages. J Immunol 137:3521-3527.
17. Fuente Mde L, Cruces J, Hernandez O, Ortega E. 2011. Strategies to improve the functions and redox state of the immune system in aged subjects. Curr Pharm Des 17:3966-3993.
18. Ghezzi P, Bonetto V. 2003. Redox proteomics: Identification of oxidatively modified proteins. Proteomics 3:1145-1153.
19. Gidday JM. 2006. Cerebral preconditioning and ischemic tolerance. Nat Rev Neurosci 7:437-448.
20. Girard S, Brough D, Lopez-Castejon G, Giles J, Rothwell NJ, Allan SM. 2013. Microglia and macrophages differentially modulate cell death after brain injury caused by oxygen deprivation in organotypic brain slices. Glia 61:813-824.
21. Grafstein B. 2011. Subverting the hegemony of the synapse: Complicity of neurons, astrocytes, and vasculature in spreading depression and pathology of the cerebral cortex. Brain Res Rev 66:123-132.
22. Grinberg YY, Milton JG, Kraig RP. 2011. Spreading depression sends microglia on Lévy flights. PLoS One 6:e19294.
23. Grinberg YY, van Drongelen W, Kraig RP. 2012. Insulin-like growth factor-1 lowers spreading depression susceptibility and reduces oxidative stress. J Neurochem 122:221-229.
24. Grinberg YY, Dibbern ME, Levasseur VA, Kraig RP. 2013. Insulin-like growth factor-1 abrogates microglial oxidative stress and the TNFα responses to spreading depression. J Neurochem 126:662-672.
25. Guedes RC, Monterio JS, Teodosio NR. 1996. Malnutrition and brain function: experimental studies using the phenomenon of cortical spreading depression. Rev Bras Biol 56:293-301.
26. Herring A, Blome M, Ambree O, Sachser N, Paulus W, Keyvani K. 2010. Reduction of cerebral oxidative stress following environmental enrichment in mice with Alzheimer-like pathology. Brain Pathol 20:166-175.
27. Hounsgaard J, Nicholson C. 1983. Potassium accumulation around individual Purkinje cells in cerebellar slices from the guinea-pig. J Physiol 340:359-388.
28. Hulse RE, Swenson WG, Kunkler PE, White DM, Kraig RP. 2008. Monomeric IgG is neuroprotective via enhancing microglial recycling endocytosis and TNF-alpha. J Neurosci 25:3952-3961.
29. Kariko K, Weissman D, Welsh FA. 2004. Inhibition of toll-like receptor and cytokine signaling - A unifying theme in ischemic tolerance. J Cereb Blood Flow Metab 24:1288-1304.
30. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG. 2009. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci 29:13435-13444.
31. Kobayashi K, Imagama S, Ohgomori T, Hirano K, Uchimura K, Sakamoto K, Hirakawa A, Takeuchi H, Suzumura A, Ishiguro N, Kadomatsu K. 2013. Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis 4:e525.
32. Kovacs R, Papageorgiou I, Heinemann U. 2011. Slice cultures as a model to study neurovascular coupling and blood brain barrier in vitro. Cardiovasc Psychiatry Neurol 2011:646958.
33. Kraig RP, Dong LM, Thisted R, Jaeger CB. 1991. Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J Neurosci 11:2187-2198.
34. Kraig RP, Mitchell HM, Cristie-Pope B, Kunkler PE, White DM, Tang YP, Langan G. 2010. TNFα and microglial hermetic involvement in neurological health & migraine. Dose Response 8:389-413.
35. Kreutz S, Koch M, Bottger C, Ghadban C, Korf HW, Dehghani F. 2009. 2-Arachidonoylglycerol elicits neuroprotective effects on excitotoxically lesioned dentate gyrus granule cells via abnormal-cannabidiol-sensitive receptors on microglial cells. Glia 57:286-294.
36. Kruger H, Luhmann HJ, Heinemann U. 1996. Repetitive spreading depression causes selective suppression of GABAergic function. Neuroreport 10:2651-2656.
37. Kudo C, Nozari A, Moskowitz MA, Ayata C. 2008. The impact of anesthetics and hyperoxia on cortical spreading depression. Exp Neurol 212:201-206.
38. Kunkler PE, Hulse RE, Kraig RP. 2004. Multiplexed cytokine protein expression profiles from spreading depression in hippocampal organotypic cultures. J Cereb Blood Flow Metab 24:829-839.
39. Kunkler PE, Hulse RE, Schmitt MW, Nicholson C, Kraig RP. 2005. Optical current source density analysis in hippocampal organotypic culture shows that spreading depression occurs with uniquely reversing currents. J Neurosci 25:3952-3961.
40. Kunkler PE, Kraig RP. 1997. Reactive astrocytosis from excitotoxic injury in hippocampal organ culture parallels that seen in vivo. J Cereb Blood Flow Metab 17:26-43.
41. Kunkler PE, Kraig RP. 1998. Calcium waves precede electrophysiological changes of spreading depression in hippocampal organ cultures. J Neurosci 18:3416-3425.
42. 2+ rise in hippocampal organ culture. Hippocampus 14:356-367.
43. Lapilover EG, Lippmann K, Salar S, Maslarova A, Dreier JP, Heinemann U, Friedman A. 2012. Peri-infarct blood-brain barrier dysfunction facilitates induction of spreading depolarization associated with epileptiform discharges. Neurobiol Dis 48:495-506.
44. Liao B, Zhao W, Beers DR, Henkel JS, Appel SH. 2012. Transformation from a neuroprotective to a neurotoxic microglial phenotype in a mouse model of ALS. Exp Neurol 237:147-152.
45. Liu XF, Fawcett JR, Thorne RG, Defor TA, Frey WH II. 2001. Intranasal administration of insulin-like growth factor-I bypasses the blood-brain barrier and protects against focal cerebral ischemic damage. J Neurol Sci 187:91-97.
46. Lochhead JJ, Thorne RG. 2012. Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64:614-628.
47. Maiorino C, Khorooshi R, Ruffini F, Lobner M, Bergami A, Garzetti L, Martino G, Owen T, Furlan R. 2013. Lentiviral-mediated administration of IL-25 in the CNS induces alternative activation of microglia. Gene Ther 20:487-496.
48. Mandavilli BS, Janes MS. 2010. Detection of intracellular glutathione using ThiolTracker violet stain and fluorescence microscopy. Curr Protoc Cytom Chapter 9:Unit 9.35.
49. Marashi V, Barnekow A, Ossendorf E, Sachser N. 2003. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Horm Behav 43:281-292.
50. Markovic DS, Glass R, Synowitz M, van Rooijen N, Kettenmann H. 2005. Microglia stimulate the invasiveness of glioma cells by increasing the activity of metalloprotease-2. J Neuropathol Exp Neurol 64:754-762.
51. Martins-Ferreira H, Nedergaard M, Nicholson C. 2000. Perspectives on spreading depression. Brain Res Rev 32:215-234.
52. Maheshwari A, Janssens K, Bogie J, Van Den Haute C, Struys T, Lambrichts I, Baekelandt V, Stinissen P, Hendriks JJ, Slaets H, Hellings N. 2013. Local overexpression of interleukin-11 in the central nervous system limits demyelination and enhances remyelination. Mediators Inflamm 2013:685317.
53. Mitchell HM, White DM, Domowicz MS, Kraig RP. 2011. Cold pre-conditioning neuroprotection depends on TNFα and is enhanced by blockade of interleukin-11. J Neurochem 117:187-196.
54. Mitchell HM, White DM, Kraig RP. 2010. Strategies for study of neuroprotection from cold-preconditioning. J Vis Exp 43:2192.
55. Obiang P, Maubert E, Bardou I, Nicole O, Launay S, Bezin L, Vivien D, Agin V. 2011. Enriched housing reverses age-associated impairment of cognitive functions and tPA-dependent maturation of BDNF. Neurobiol Learn Mem 96:121-129.
56. Olson AK, Eadie BD, Ernst C, Christie BR. 2006. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16:250-260.
57. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
58. Pietrobon D, Moskowitz MA. 2013. Pathophysiology of migraine. Annu Rev Physiol 75:365-391.
59. Pomper JK, Haack S, Petzold GC, Buchheim K, Gabriel S, Hoffman U, Heinemann U. 2006. Repetitive spreading depression-like events result in cell damage in juvenile hippocampal slice cultures maintained in normoxia. J Neurophysiol 95:355-368.
60. A receptors. J Neurosci 33:15879-15893.
61. Pusic AD, Grinberg YY, Mitchell HM, Kraig RP. 2011. Modeling neural immune signaling of episodic and chronic migraine using spreading depression in vitro. J Vis Exp 52:2910.
62. Pusic AD, Kraig RP. 2014. Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination. Glia 62:284-299.
63. Pusic AD, Pusic KM, Kraig RP. 2014. IFNγ-stimulated dendritic cell exosomes as a potential therapeutic for remyelination. J Neuroimmunol 266:12-23.
64. Pusic KM, Pusic AD, Kraig RP. 2013. Microglia are essential for spreading depression. Soc Neurosci 39:812.02.
65. Radak Z, Chung HY, Goto S. 2008. Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44:153-159.
66. Ransohoff RM, Perry VH. 2009. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119-145.
67. Rodriquez M, Sabate M, Rodriqez-Sabate C, Morales I. 2013. The role of non-synaptic extracellular glutamate. Brain Res Bull 93:17-26.
68. Roundtree RB, Mandl SJ, Nachtwey JM, Dalpozzo K, Do L, Lombardo JR, Schoonmaker PL, Brinkmann K, Dirmeier U, Laus R, Delcayre A. 2011. Exosome targeting of tumor antigens expressed by cancer vaccines can improve antigen immunogenicity and therapeutic efficacy. Cancer Res 71:5235-5244.
69. Sasaki S, Matsuura T, Takahashi R, Iwasa T, Watanabe H, Shirai K, Nakamoto H, Goto S, Akita S, Kobayashi Y. 2013. Effects of regular exercise on neutrophil functions, oxidative stress parameters and antibody responses against 4-hydroxy-2-nonenal adducts in middle aged humans. Exerc Immunol Rev 19:60-71.
70. Schuchmann S, Meierkord H, Stenkamp K, Breustedt J, Windmuller O, Heinemann U, Buchheim K. 2002. Synaptic and nonsynaptic ictogenesis occurs at different temperatures in submerged and interface rat brain slices. J Neurophysiol 87:2929-2935.
71. Shatillo A, Koroleva K, Giniatullina R, Naumenko N, Slastnikova AA, Aliev AA, Bart RR, Atalay M, Gu C, Khazipov B, Grohn O, Ginniatullin R. 2013. Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system. Neuroscience 253:341-349.
72. Sievers J, Schmidtmayer J, Parwaresch R. 1994. Blood monocytes and spleen macrophages differentiate into microglia-like cells when cultured on astrocytes. Ann Anat 176:45-51.
73. Snow RW, Taylor CP, Dudek FE. 1983. Electrophysiological and optical changes in slices of rat hippocampus during spreading depression. J Neurophysiol 50:561-572.
74. Somjen GG. 2001. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065-1096.
75. Stellwagen D, Beattie EC, Seo JY, Malenka RC. 2005. Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci 25:3219-3228.
76. Stenzel-Poore MP, Stevens SL, King JS, Simon RP. 2007. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38:680-685.
77. Tetrault S, Chever O, Sik A, Amzica F. 2008. Opening of the blood-brain barrier during isoflurane anesthesia. Eur J Neurosci 28:1330-1341.
78. Thorne RG, Pronk GJ, Padmanabhan V, Frey WH II. 2004. Delivery of insulin-like growth factor-1 to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127:481-496.
79. Trepicchio WL, Bozza M, Pedneault G, Dorner AJ. 1996. Recombinant human IL-11 attenuates the inflammatory response through down-regulation of proinflammatory cytokine release and nitric oxide production. J Immunol 157:3627-3634.
80. Trepicchio WL, Dorner AJ. 1998. The therapeutic utility of interleukin-11 in the treatment of inflammatory disease. Expert Opin Investig Drugs 7:1501-1504.
81. Tsuda M, Beggs S, Salter MW, Inoue K. 2013. Microglia and intractable chronic pain. Glia 61:55-61.
82. van Praag H, Kempermann G, Gage FH. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
83. van Rooijen N. 1989. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods 124:1-6.
84. Viggiano A, Viggiano E, Valentino I, Monda M, De Luca B. 2011. Cortical spreading depression affects reactive oxygen species production. Brain Res 1368:11-18.
85. Vinet J, Weering HR, Heinrich A, Kalin RE, Wegner A, Brouwer N, Heppner FL, Rooijen Nv, Boddeke HW, Biber K. 2012. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation 9:27.
86. Williamson LL, Chao A, Bilbo SD. 2012. Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus. Brain Behav Immun 26:500-510.
87. Zhang XC, Kainz V, Burstein R, Levy D. 2011. Tumor necrosis factor-α induces sensitization of meningeal noiciceptors mediated via local COX and p38 MAP actions. Pain 152:140-149.
88. Zhang Y, Taveggia C, Melendez-Vasquez C, Einheber S, Raine CS, Salzer JL, Brosnan CF, John GR. 2006. Interleukin-11 potentiates oligodendrocyte survival and maturation, and myelin formation. J Neurosci 26:12174-12185.