Conditional ablation of myeloid TNF increases lesion volume after experimental stroke in mice, possibly via altered ERK1/2 signaling

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Clausen, Bettina Hjelm ^a   Degn, Matilda ^b   Sivasaravanaparan, Mithula ^a   Fogtmann, Torben ^a   Andersen, Maria Gammelstrup ^a   Trojanowsky, Michelle D ^c   Gao, Han ^c   Hvidsten, Svend ^d   Baun, Christina ^d   Deierborg, Tomas ^e   Finsen, Bente ^a   Kristensen, Bjarne Winther ^a,d   Bak, Sara Thornby ^a   Meyer, Morten ^a   Lee, Jae ^c   Nedospasov, Sergei A ^f   Brambilla, Roberta ^c   Lambertsen, Kate Lykke ^a,d  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b Rigshospitalet   (Denmark)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e LUND UNIVERSITY   (Sweden)

^f ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 5; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ANIMAL; BONE MARROW CELL; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; DISEASE MODEL; INFLAMMATION; KNOCKOUT MOUSE; LEUKOCYTE; MALE; MAPK SIGNALING; METABOLISM; MICROGLIA; MOUSE; NEUROPROTECTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN ISCHEMIA; CYTOKINES; DISEASE MODELS, ANIMAL; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-5; INTERLEUKIN-6; LEUKOCYTES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MICROGLIA; MYELOID CELLS; NEUROPROTECTION; SIGNAL TRANSDUCTION; STROKE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84977626203     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29291     Document Type: Article

References (61)

1. Schwartz, M., Butovsky, O., Bruck, W. & Hanisch, U. K. Microglial phenotype: is the commitment reversible? Trends Neurosci 29, 68-74 (2006).
2. Lambertsen, K. L., Biber, K. & Finsen, B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab 32, 1677-1698, doi: 10.1038/jcbfm.2012.88 (2012).
3. Clausen, B. et al. Systemically administered anti-TNF therapy ameliorates functional outcomes after focal cerebral ischemia. J Neuroinflammation 11, 203, doi: 10.1186/PREACCEPT-2982253041347736 (2014).
4. Lambertsen, K. L. et al. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29, 1319-1330, doi: 10.1523/JNEUROSCI.5505-08.2009 (2009).
5. Madsen P. M. et al. Genetic ablation of soluble tumor necrosis factor with preservation of membrane tumor necrosis factor is associated with neuroprotection after focal cerebral ischemia. J Cereb Blood Flow Metab doi 10.1177/0271678X15610339 (2015)
6. Novrup, H. G. et al. Central but not systemic administration of XPro1595 is therapeutic following moderate spinal cord injury in mice. J Neuroinflammation 11, 159, doi: 10.1186/s12974-014-0159-6 (2014).
7. Probert, L. TNF and its receptors in the CNS: The essential, the desirable and the deleterious effects. Neuroscience, doi: 10.1016/j. neuroscience.2015.06.038 (2015).
8. Alexopoulou, L. et al. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur J Immunol 36, 2768-2780, doi: 10.1002/eji.200635921 (2006).
9. Brambilla, R. et al. Inhibition of soluble tumour necrosis factor is therapeutic in experimental autoimmune encephalomyelitis and promotes axon preservation and remyelination. Brain 134, 2736-2754, doi: 10.1093/brain/awr199 (2011).
10. Chen, G. & Goeddel, D. V. TNF-R1 signaling: a beautiful pathway. Science 296, 1634-1635 (2002).
11. Subramaniam, S. & Unsicker, K. ERK and cell death: ERK1/2 in neuronal death. FEBS J 277, 22-29, doi: 10.1111/j.1742-4658.2009.07367.x (2010).
12. Marchetti, L., Klein, M., Schlett, K., Pfizenmaier, K. & Eisel, U. L. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 279, 32869-32881 (2004).
13. Taoufik, E. et al. Transmembrane tumour necrosis factor is neuroprotective and regulates experimental autoimmune encephalomyelitis via neuronal nuclear factor-kappaB. Brain 134, 2722-2735, doi: 10.1093/brain/awr203 (2011).
14. Taoufik, E. et al. FLIP(L) protects neurons against in vivo ischemia and in vitro glucose deprivation-induced cell death. J Neurosci 27, 6633-6646 (2007).
15. Bruce, A. J. et al. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med 2, 788-794 (1996).
16. Pradillo, J. M. et al. TNFR1 upregulation mediates tolerance after brain ischemic preconditioning. J Cereb Blood Flow Metab 25, 193-203 (2005).
17. Frank, M. & Wolburg, H. Cellular reactions at the lesion site after crushing of the rat optic nerve. Glia 16, 227-240, doi: 10.1002/ (SICI)1098-1136(199603)16:3<227::AID-GLIA5>3.0.CO;2-Z (1996).
18. Atarashi, R. et al. Abnormal activation of glial cells in the brains of prion protein-deficient mice ectopically expressing prion proteinlike protein, PrPLP/Dpl. Mol Med 7, 803-809 (2001).
19. Hedtjarn, M., Mallard, C. & Hagberg, H. Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia. J Cereb Blood Flow Metab 24, 1333-1351, doi: 10.1097/01.WCB.0000141559.17620.36 (2004).
20. Clausen, B. H., Lambertsen, K. L. & Finsen, B. Glyceraldehyde-3-phosphate dehydrogenase versus toluidine blue as a marker for infarct volume estimation following permanent middle cerebral artery occlusion in mice. Exp Brain Res 175, 60-67, doi: 10.1007/ s00221-006-0526-3 (2006).
21. Goel, G. et al. Combined effect of tumor necrosis factor (TNF)-alpha and heat shock protein (HSP)-70 in reducing apoptotic injury in hypoxia: a cell culture study. Neurosci Lett 483, 162-166, doi: 10.1016/j.neulet.2010.07.069 (2010).
22. Lambertsen, K. L., Meldgaard, M., Ladeby, R. & Finsen, B. A quantitative study of microglial-macrophage synthesis of tumor necrosis factor during acute and late focal cerebral ischemia in mice. J Cereb Blood Flow Metab 25, 119-135, doi: 10.1038/sj. jcbfm.9600014 (2005).
23. Lambertsen, K. L., Gregersen, R. & Finsen, B. Microglial-macrophage synthesis of tumor necrosis factor after focal cerebral ischemia in mice is strain dependent. J Cereb Blood Flow Metab 22, 785-797. (2002).
24. Bianchi, M., Sacerdote, P., Ricciardi-Castagnoli, P., Mantegazza, P. & Panerai, A. E. Central effects of tumor necrosis factor alpha and interleukin-1 alpha on nociceptive thresholds and spontaneous locomotor activity. Neurosci Lett 148, 76-80 (1992).
25. Golan, H., Levav, T., Mendelsohn, A. & Huleihel, M. Involvement of tumor necrosis factor alpha in hippocampal development and function. Cereb Cortex 14, 97-105 (2004).
26. Grivennikov, S. I. et al. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22, 93-104, doi: 10.1016/j.immuni.2004.11.016 (2005).
27. Lambertsen, K. L., Gregersen, R., Drojdahl, N., Owens, T. & Finsen, B. A specific and sensitive method for visualization of tumor necrosis factor in the murine central nervous system. Brain Res Brain Res Protoc 7, 175-191 (2001).
28. Gregersen, R., Lambertsen, K. & Finsen, B. Microglia and macrophages are the major source of tumor necrosis factor in permanent middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 20, 53-65 (2000).
29. Ginsberg, M. D., Reivich, M., Giandomenico, A. & Greenberg, J. H. Local glucose utilization in acute focal cerebral ischemia: local dysmetabolism and diaschisis. Neurology 27, 1042-1048 (1977).
30. Yuan, H. et al. Spatiotemporal uptake characteristics of [18]f-2-fluoro-2-deoxy-d-glucose in a rat middle cerebral artery occlusion model. Stroke 44, 2292-2299, doi: 10.1161/STROKEAHA.113.000903 (2013).
31. Schroeter, M. et al. Neuroinflammation extends brain tissue at risk to vital peri-infarct tissue: a double tracer [11C]PK11195-and [18F]FDG-PET study. J Cereb Blood Flow Metab 29, 1216-1225, doi: 10.1038/jcbfm.2009.36 (2009).
32. Subramaniam, S. & Unsicker, K. Extracellular signal-regulated kinase as an inducer of non-apoptotic neuronal death. Neuroscience 138, 1055-1065, doi: 10.1016/j.neuroscience.2005.12.013 (2006).
33. Tran, S. E., Holmstrom, T. H., Ahonen, M., Kahari, V. M. & Eriksson, J. E. MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J Biol Chem 276, 16484-16490, doi: 10.1074/jbc.M010384200 (2001).
34. Barbin, G., Roisin, M. P. & Zalc, B. Tumor necrosis factor alpha activates the phosphorylation of ERK, SAPK/JNK, and P38 kinase in primary cultures of neurons. Neurochem Res 26, 107-112 (2001).
35. Rousseau, S. et al. TPL2-mediated activation of ERK1 and ERK2 regulates the processing of pre-TNF alpha in LPS-stimulated macrophages. J Cell Sci 121, 149-154, doi: 10.1242/jcs.018671 (2008).
36. Humphreys, B. D. & Dubyak, G. R. Modulation of P2X7 nucleotide receptor expression by pro-and anti-inflammatory stimuli in THP-1 monocytes. J Leukoc Biol 64, 265-273 (1998).
37. Suzuki, T. et al. Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J Neurosci 24, 1-7, doi: 10.1523/JNEUROSCI.3792-03.2004 (2004).
38. Ritzel, R. M. et al. Functional differences between microglia and monocytes after ischemic stroke. J Neuroinflammation 12, 106, doi: 10.1186/s12974-015-0329-1 (2015).
39. Denes, A. et al. Experimental stroke-induced changes in the bone marrow reveal complex regulation of leukocyte responses. J Cereb Blood Flow Metab 31, 1036-1050, doi: 10.1038/jcbfm.2010.198 (2011).
40. Brambilla, R., Couch, Y. & Lambertsen, K. L. The effect of stroke on immune function. Mol Cell Neurosci 10.1016/j. mcn.2012.08.011 (2012)
41. Clausen, B. H. et al. Cell therapy centered on IL-1Ra is neuroprotective in experimental stroke. Acta Neuropathol, doi: 10.1007/ s00401-016-1541-5 (2016).
42. Denes, A. et al. Central autonomic control of the bone marrow: multisynaptic tract tracing by recombinant pseudorabies virus. Neuroscience 134, 947-963, doi: 10.1016/j.neuroscience.2005.03.060 (2005).
43. Prass, K. et al. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 198, 725-736, doi: 10.1084/jem.20021098 (2003).
44. Offner, H. et al. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol 176, 6523-6531 (2006).
45. Izci, Y. Splenectomy may be a prophylactic treatment for cerebral ischemia? Med Hypotheses 75, 347-349, doi: 10.1016/j. mehy.2010.03.018 (2010).
46. Solovjov, D. A., Pluskota, E. & Plow, E. F. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem 280, 1336-1345, doi: 10.1074/jbc.M406968200 (2005).
47. Campbell, S. J. et al. Immunomodulatory effects of etanercept in a model of brain injury act through attenuation of the acute-phase response. J Neurochem 103, 2245-2255, doi: 10.1111/j.1471-4159.2007.04928.x (2007).
48. Garcia, J. H. et al. Influx of leukocytes and platelets in an evolving brain infarct (Wistar rat). Am J Pathol 144, 188-199 (1994).
49. Cho, I. H. et al. Role of microglial IKKbeta in kainic acid-induced hippocampal neuronal cell death. Brain 131, 3019-3033, doi: 10.1093/brain/awn230 (2008).
50. Arenkiel, B. R. et al. Activity-induced remodeling of olfactory bulb microcircuits revealed by monosynaptic tracing. PLoS One 6, e29423, doi: 10.1371/journal.pone.0029423 (2011).
51. Zhu, Y. et al. Hematogenous macrophage depletion reduces the fibrotic scar and increases axonal growth after spinal cord injury. Neurobiol Dis 74, 114-125, doi: 10.1016/j.nbd.2014.10.024 (2015).
52. Lambertsen, K. L. et al. Genetic KCa3.1-deficiency produces locomotor hyperactivity and alterations in cerebral monoamine levels. PLoS One 7, e47744, doi: 10.1371/journal.pone.0047744 (2012).
53. Lanz, B., Poitry-Yamate, C. & Gruetter, R. Image-Derived Input Function from the Vena Cava for 18F-FDG PET Studies in Rats and Mice. Journal of nuclear medicine : official publication, Society of Nuclear Medicine 55, 1380-1388, doi: 10.2967/jnumed.113.127381 (2014).
54. Fueger, B. J. et al. Impact of animal handling on the results of 18F-FDG PET studies in mice. Journal of nuclear medicine: official publication, Society of Nuclear Medicine 47, 999-1006 (2006).
55. Metz, G. A. & Whishaw, I. Q. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore-and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115, 169-179 (2002).
56. Lin, T. N., He, Y. Y., Wu, G., Khan, M. & Hsu, C. Y. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24, 117-121 (1993).
57. Clausen, B. H. et al. Interleukin-1beta and tumor necrosis factor-alpha are expressed by different subsets of microglia and macrophages after ischemic stroke in mice. J Neuroinflammation 5, 46, doi: 10.1186/1742-2094-5-46 (2008).
58. Brambilla, R. et al. Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 62, 452-467, doi: 10.1002/glia.22616 (2014).
59. Bracchi-Ricard, V. et al. Inhibition of astroglial NF-kappaB enhances oligodendrogenesis following spinal cord injury. J Neuroinflammation 10, 92, doi: 10.1186/1742-2094-10-92 (2013).
60. Lambertsen, K. L. et al. No effect of ablation of surfactant protein-D on acute cerebral infarction in mice. J Neuroinflammation 11, 123, doi: 10.1186/1742-2094-11-123 (2014).
61. Hermansen, S. K., Christensen, K. G., Jensen, S. S. & Kristensen, B. W. Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem 59, 391-407, doi: 10.1369/0022155411400867 (2011).