A neuroprotective role for microglia in prion diseases

Journal of Experimental Medicine

Volumn 213, Issue 6, 2016, Pages 1047-1059

  Zhu, Caihong ^a   Herrmann, Uli S ^a   Falsig, Jeppe ^a   Abakumova, Irina ^a   Nuvolone, Mario ^a   Schwarz, Petra ^a   Frauenknecht, Katrin ^a   Rushing, Elisabeth J ^a   Aguzzi, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; GANCICLOVIR; INTERLEUKIN 34; PRION PROTEIN; PROTEIN KINASE; THYMIDINE KINASE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-34, MOUSE; PRION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DETERIORATION; DISEASE COURSE; HERPES SIMPLEX VIRUS; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRION DISEASE; PRIORITY JOURNAL; ANIMAL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PRION;

ANIMALS; INTERLEUKINS; MICE; MICE, KNOCKOUT; MICROGLIA; PRION DISEASES; PRIONS;

EID: 84971501084     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151000     Document Type: Article

References (43)

1. Aguzzi, A., and J. Falsig. 2012. Prion propagation, toxicity and degradation. Nat. Neurosci. 15:936-939. http://dx.doi.org/10.1038/nn.3120
2. Aguzzi, A., B.A. Barres, and M.L. Bennett. 2013a. Microglia: scapegoat, saboteur, or something else? Science. 339:156-161. http://dx.doi.org/10.1126/science.1227901
3. Aguzzi, A., M. Nuvolone, and C. Zhu. 2013b. The immunobiology of prion diseases. Nat. Rev. Immunol. 13:888-902. http://dx.doi.org/10.1038/nri3553
4. Aguzzi, A., J. Kranich, and N.J. Krautler. 2014. Follicular dendritic cells: origin, phenotype, and function in health and disease. Trends Immunol. 35:105-113. http://dx.doi.org/10.1016/j.it.2013.11.001
5. Alliot, F., I. Godin, and B. Pessac. 1999. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res. Dev. Brain Res. 117:145-152. http://dx.doi.org/10.1016/S0165-3806(99)00113-3
6. Baker, C.A., D. Martin, and L. Manuelidis. 2002. Microglia from Creutzfeldt-Jakob disease-infected brains are infectious and show specific mRNA activation profiles. J. Virol. 76:10905-10913. http://dx.doi.org/10.1128/JVI.76.21.10905-10913.2002
7. Brown, D.R., B. Schmidt, and H.A. Kretzschmar. 1996. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature. 380:345-347. http://dx.doi.org/10.1038/380345a0
8. Chen, S.K., P. Tvrdik, E. Peden, S. Cho, S. Wu, G. Spangrude, and M.R. Capecchi. 2010. Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell. 141:775-785. http://dx.doi.org/10.1016/j.cell.2010.03.055
9. Davalos, D., J. Grutzendler, G. Yang, J.V. Kim, Y. Zuo, S. Jung, D.R. Littman, M.L. Dustin, and W.B. Gan. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8:752-758. http://dx.doi.org/10.1038/nn1472
10. Derecki, N.C., J.C. Cronk, Z. Lu, E. Xu, S.B. Abbott, P.G. Guyenet, and J. Kipnis. 2012. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature. 484:105-109. http://dx.doi.org/10.1038/nature10907
11. Drabkin, D.L., and J.H. Austin. 1935. Preparations from washed blood cells; nitric oxide hemoglobin and sulfhemoglobin. J. Biol. Chem. 112:51-65.
12. Falsig, J., and A. Aguzzi. 2008. The prion organotypic slice culture assay--POS CA. Nat. Protoc. 3:555-562. http://dx.doi.org/10.1038/nprot.2008.13
13. Falsig, J., C. Julius, I. Margalith, P. Schwarz, F.L. Heppner, and A. Aguzzi. 2008. A versatile prion replication assay in organotypic brain slices. Nat. Neurosci. 11:109-117. http://dx.doi.org/10.1038/nn2028
14. Falsig, J., T. Sonati, U.S. Herrmann, D. Saban, B. Li, K. Arroyo, B. Ballmer, P.P. Liberski, and A. Aguzzi. 2012. Prion pathogenesis is faithfully reproduced in cerebellar organotypic slice cultures. PLoS Pathog. 8:e1002985. http://dx.doi.org/10.1371/journal.ppat.1002985
15. Fischer, M., T. Rülicke, A. Raeber, A. Sailer, M. Moser, B. Oesch, S. Brandner, A. Aguzzi, and C. Weissmann. 1996. Prion protein (PrP) with aminoproximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15:1255-1264.
16. Giese, A., D.R. Brown, M.H. Groschup, C. Feldmann, I. Haist, and H.A. Kretzschmar. 1998. Role of microglia in neuronal cell death in prion disease. Brain Pathol. 8:449-457. http://dx.doi.org/10.1111/j.1750-3639.1998.tb00167.x
17. Ginhoux, F., M. Greter, M. Leboeuf, S. Nandi, P. See, S. Gokhan, M.F. Mehler, S.J. Conway, L.G. Ng, E.R. Stanley, et al. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 330:841-845. http://dx.doi.org/10.1126/science.1194637
18. Gómez-Nicola, D., N.L. Fransen, S. Suzzi, and V.H. Perry. 2013. Regulation of microglial proliferation during chronic neurodegeneration. J. Neurosci. 33:2481-2493. http://dx.doi.org/10.1523/JNEUROSCI.4440-12.2013
19. Gómez-Nicola, D., S.T. Schetters, and V.H. Perry. 2014. Differential role of CCR2 in the dynamics of microglia and perivascular macrophages during prion disease. Glia. 62:1041-1052. http://dx.doi.org/10.1002/glia.22660
20. Grathwohl, S.A., R.E. Kälin, T. Bolmont, S. Prokop, G. Winkelmann, S.A. Kaeser, J. Odenthal, R. Radde, T. Eldh, S. Gandy, et al. 2009. Formation and maintenance of Alzheimer's disease ß-amyloid plaques in the absence of microglia. Nat. Neurosci. 12:1361-1363. http://dx.doi.org/10.1038/nn.2432
21. Greter, M., I. Lelios, P. Pelczar, G. Hoeffel, J. Price, M. Leboeuf, T.M. Kündig, K. Frei, F. Ginhoux, M. Merad, and B. Becher. 2012. Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity. 37:1050-1060. http://dx.doi.org/10.1016/j.immuni.2012.11.001
22. Hanisch, U.K., and H. Kettenmann. 2007. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10:1387-1394. http://dx.doi.org/10.1038/nn1997
23. Heppner, F.L., M. Greter, D. Marino, J. Falsig, G. Raivich, N. Hövelmeyer, A. Waisman, T. Rülicke, M. Prinz, J. Priller, et al. 2005. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11:146-152. http://dx.doi.org/10.1038/nm1177
24. Herrmann, U.S., T. Sonati, J. Falsig, R.R. Reimann, P. Dametto, T. O'Connor, B. Li, A. Lau, S. Hornemann, S. Sorce, et al. 2015. Prion infections and anti-PrP antibodies trigger converging neurotoxic pathways. PLoS Pathog. 11:e1004662. http://dx.doi.org/10.1371/journal.ppat.1004662
25. Hughes, M.M., R.H. Field, V.H. Perry, C.L. Murray, and C. Cunningham. 2010. Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia. 58:2017-2030. http://dx.doi.org/10.1002/glia.21070
26. Jeffrey, M., C.M. Goodsir, M.E. Bruce, P.A. McBride, and C. Farquhar. 1994. Morphogenesis of amyloid plaques in 87V murine scrapie. Neuropathol. Appl. Neurobiol. 20:535-542. http://dx.doi.org/10.1111/j.1365-2990.1994.tb01007.x
27. Kierdorf, K., D. Erny, T. Goldmann, V. Sander, C. Schulz, E.G. Perdiguero, P. Wieghofer, A. Heinrich, P. Riemke, C. Hölscher, et al. 2013. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 16:273-280. http://dx.doi.org/10.1038/nn.3318
28. Klein, T.R., D. Kirsch, R. Kaufmann, and D. Riesner. 1998. Prion rods contain small amounts of two host sphingolipids as revealed by thinlayer chromatography and mass spectrometry. Biol. Chem. 379:655-666. http://dx.doi.org/10.1515/bchm.1998.379.6.655
29. Kranich, J., N.J. Krautler, J. Falsig, B. Ballmer, S. Li, G. Hutter, P. Schwarz, R. Moos, C. Julius, G. Miele, and A. Aguzzi. 2010. Engulfment of cerebral apoptotic bodies controls the course of prion disease in a mouse straindependent manner. J. Exp. Med. 207:2271-2281. http://dx.doi.org/10.1084/jem.20092401
30. Long, J.M., A.N. Kalehua, N.J. Muth, J.M. Hengemihle, M. Jucker, M.E. Calhoun, D.K. Ingram, and P.R. Mouton. 1998. Stereological estimation of total microglia number in mouse hippocampus. J. Neurosci. Methods. 84:101-108. http://dx.doi.org/10.1016/S0165-0270(98)00100-99821640
31. McHugh, D., T. O'Connor, J. Bremer, and A. Aguzzi. 2012. ZyFISH: a simple, rapid and reliable zygosity assay for transgenic mice. PLoS One. 7:e37881. http://dx.doi.org/10.1371/journal.pone.0037881
32. Mildner, A., B. Schlevogt, K. Kierdorf, C. Böttcher, D. Erny, M.P. Kummer, M. Quinn, W. Brück, I. Bechmann, M.T. Heneka, et al. 2011. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J. Neurosci. 31:11159-11171. http://dx.doi.org/10.1523/JNEUROSCI.6209-10.2011
33. Nimmerjahn, A., F. Kirchhoff, and F. Helmchen. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 308:1314-1318. http://dx.doi.org/10.1126/science.1110647
34. Paolicelli, R.C., G. Bolasco, F. Pagani, L. Maggi, M. Scianni, P. Panzanelli, M. Giustetto, T.A. Ferreira, E. Guiducci, L. Dumas, et al. 2011. Synaptic pruning by microglia is necessary for normal brain development. Science. 333:1456-1458. http://dx.doi.org/10.1126/science.1202529
35. Parkhurst, C.N., G. Yang, I. Ninan, J.N. Savas, J.R. Yates III, J.J. Lafaille, B.L. Hempstead, D.R. Littman, and W.B. Gan. 2013. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 155:1596-1609. http://dx.doi.org/10.1016/j.cell.2013.11.030
36. Rogers, J.T., J.M. Morganti, A.D. Bachstetter, C.E. Hudson, M.M. Peters, B.A. Grimmig, E.J. Weeber, P.C. Bickford, and C. Gemma. 2011. CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity. J. Neurosci. 31:16241-16250. http://dx.doi.org/10.1523/JNEUROSCI.3667-11.2011
37. Rouvinski, A., S. Karniely, M. Kounin, S. Moussa, M.D. Goldberg, G. Warburg, R. Lyakhovetsky, D. Papy-Garcia, J. Kutzsche, C. Korth, et al. 2014. Live imaging of prions reveals nascent PrPSc in cell-surface, raft-associated amyloid strings and webs. J. Cell Biol. 204:423-441. http://dx.doi.org/10.1083/jcb.201308028
38. Schafer, D.P., E.K. Lehrman, A.G. Kautzman, R. Koyama, A.R. Mardinly, R. Yamasaki, R.M. Ransohoff, M.E. Greenberg, B.A. Barres, and B. Stevens. 2012. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron. 74:691-705. http://dx.doi.org/10.1016/j.neuron.2012.03.026
39. Schulz, C., E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S.E. Jacobsen, J.W. Pollard, et al. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 336:86-90. http://dx.doi.org/10.1126/science.1219179
40. Sonati, T., R.R. Reimann, J. Falsig, P.K. Baral, T. O'Connor, S. Hornemann, S. Yaganoglu, B. Li, U.S. Herrmann, B. Wieland, et al. 2013. The toxicity of antiprion antibodies is mediated by the flexible tail of the prion protein. Nature. 501:102-106. http://dx.doi.org/10.1038/nature12402
41. Wang, Y., K.J. Szretter, W. Vermi, S. Gilfillan, C. Rossini, M. Cella, A.D. Barrow, M.S. Diamond, and M. Colonna. 2012. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13:753-760. http://dx.doi.org/10.1038/ni.2360
42. Williams, A., P.J. Lucassen, D. Ritchie, and M. Bruce. 1997. PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Exp. Neurol. 144:433-438. http://dx.doi.org/10.1006/exnr.1997.6424
43. Zhan, Y., R.C. Paolicelli, F. Sforazzini, L. Weinhard, G. Bolasco, F. Pagani, A.L. Vyssotski, A. Bifone, A. Gozzi, D. Ragozzino, and C.T. Gross. 2014. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17:400-406. http://dx.doi.org/10.1038/nn.3641