Forebrain microglia from wild-type but not adult 5xFAD mice prevent amyloid-β plaque formation in organotypic hippocampal slice cultures

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Hellwig, Sabine ^a   Masuch, Annette ^a   Nestel, Sigrun ^b   Katzmarski, Natalie ^b   Meyer Luehmann, Melanie ^b   Biber, Knut ^a,c  

^a Department of Psychiatry and Psychotherapy ^*  (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

AGE; ALZHEIMER DISEASE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DISEASE RESISTANCE; FEMALE; FOREBRAIN; HIPPOCAMPUS; MALE; METABOLISM; MICROGLIA; MICROTOMY; MOUSE; PATHOLOGY; PHYSIOLOGY; PLAQUE, AMYLOID; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BIOLOGICAL TRANSPORT; DISEASE MODELS, ANIMAL; DISEASE RESISTANCE; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROTOMY; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; PROSENCEPHALON; TISSUE CULTURE TECHNIQUES;

EID: 84942945616     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14624     Document Type: Article

References (45)

1. Gilbert, B. J. The role of amyloid β in the pathogenesis of Alzheimers disease. J. Clin. Pathol. 66, 362-366 (2013).
2. Karran, E., Mercken, M. & De Strooper, B. The amyloid cascade hypothesis for Alzheimers disease: An appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 10, 698-712 (2011).
3. Malm, T. M., Jay, T. R. & Landreth, G. E. The Evolving Biology of Microglia in Alzheimers Disease. Neurother. J. Am. Soc. Exp. Neurother. (2014). doi: 10.1007/s13311-014-0316-8
4. doi: 10.1007/s13311-014-0316-8. 4. Prokop, S., Miller, K. R. & Heppner, F. L. Microglia actions in Alzheimers disease. Acta Neuropathol. (Berl.) 126, 461-477 (2013).
5. Fleisher-Berkovich, S. et al. Distinct modulation of microglial amyloid β phagocytosis and migration by neuropeptides (i). J. Neuroinflammation 7, 61 (2010).
6. Fu, H. et al. Complement component C3 and complement receptor type 3 contribute to the phagocytosis and clearance of fibrillar Aβ by microglia. Glia 60, 993-1003 (2012).
7. Griciuc, A. et al. Alzheimers disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron 78, 631-643 (2013).
8. Mandrekar, S. et al. Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J. Neurosci. Off. J. Soc. Neurosci. 29, 4252-4262 (2009).
9. Grathwohl, S. A. et al. Formation and maintenance of Alzheimers disease beta-Amyloid plaques in the absence of microglia. Nat. Neurosci. 12, 1361-1363 (2009).
10. Beutner, C. et al. Engineered stem cell-derived microglia as therapeutic vehicle for experimental autoimmune encephalomyelitis. Gene Ther. 20, 797-806 (2013).
11. Biber, K., Owens, T. & Boddeke, E. What is microglia neurotoxicity (Not)? Glia 62, 841-854 (2014).
12. Butovsky, O. et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131-143 (2014).
13. Hellwig, S., Heinrich, A. & Biber, K. The brains best friend: microglial neurotoxicity revisited. Front. Cell. Neurosci. 7, 71 (2013).
14. Hickman, S. E. et al. The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16, 1896-1905 (2013).
15. Elmore, M. R. P. et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82, 380-397 (2014).
16. Varvel, N. H. et al. Microglial repopulation model reveals a robust homeostatic process for replacing CNS myeloid cells. Proc. Natl. Acad. Sci. USA 109, 18150-18155 (2012).
17. Bahr, B. A. Long-Term hippocampal slices: A model system for investigating synaptic mechanisms and pathologic processes. J. Neurosci. Res. 42, 294-305 (1995).
18. Stoppini, L., Buchs, P. A. & Muller, D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182 (1991).
19. Mewes, A., Franke, H. & Singer, D. Organotypic brain slice cultures of adult transgenic P301S mice-A model for tauopathy studies. PloS One 7, e45017 (2012).
20. Braithwaite, S. P. et al. Inhibition of c-Jun kinase provides neuroprotection in a model of Alzheimers disease. Neurobiol. Dis. 39, 311-317 (2010).
21. Alberdi, E. et al. Amyloid beta oligomers induce Ca2+ dysregulation and neuronal death through activation of ionotropic glutamate receptors. Cell Calcium 47, 264-272 (2010).
22. Webster, S. J., Bachstetter, A. D., Nelson, P. T., Schmitt, F. A. & Van Eldik, L. J. Using mice to model Alzheimers dementia: An overview of the clinical disease and the preclinical behavioral changes in 10 mouse models. Front. Genet. 5, 88 (2014).
23. Jucker, M. & Walker, L. C. Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501, 45-51 (2013).
24. Kane, M. D. et al. Evidence for seeding of beta-Amyloid by intracerebral infusion of Alzheimer brain extracts in beta-Amyloid precursor protein-Transgenic mice. J. Neurosci. Off. J. Soc. Neurosci. 20, 3606-3611 (2000).
25. Meyer-Luehmann, M. et al. Exogenous induction of cerebral beta-Amyloidogenesis is governed by agent and host. Science 313, 1781-1784 (2006).
26. Vinet, J. et al. Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J. Neuroinflammation 9, 27 (2012).
27. Ji, K., Akgul, G., Wollmuth, L. P. & Tsirka, S. E. Microglia actively regulate the number of functional synapses. PloS One 8, e56293 (2013).
28. Kierdorf, K. et al. Microglia emerge from erythromyeloid precursors via Pu.1-And Irf8-dependent pathways. Nat. Neurosci. 16, 273-280 (2013).
29. DAndrea, M. R., Nagele, R. G., Wang, H. Y., Peterson, P. A. & Lee, D. H. Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimers disease. Histopathology 38, 120-134 (2001).
30. Sturchler-Pierrat, C. et al. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. USA 94, 13287-13292 (1997).
31. Radde, R. et al. Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep. 7, 940-946 (2006).
32. Oakley, H. et al. Intraneuronal beta-Amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimers disease mutations: potential factors in amyloid plaque formation. J. Neurosci. Off. J. Soc. Neurosci. 26, 10129-10140 (2006).
33. Lee, J.-H. et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158 (2010).
34. Pickford, F. et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J. Clin. Invest. 118, 2190-2199 (2008).
35. Lucin, K. M. et al. Microglial beclin 1 regulates retromer trafficking and phagocytosis and is impaired in Alzheimers disease. Neuron 79, 873-886 (2013).
36. Hickman, S. E. & El Khoury, J. TREM2 and the neuroimmunology of Alzheimers disease. Biochem. Pharmacol. 88, 495-498 (2014).
37. Krabbe, G. et al. Functional impairment of microglia coincides with Beta-Amyloid deposition in mice with Alzheimer-like pathology. PloS One 8, e60921 (2013).
38. Orre, M. et al. Isolation of glia from Alzheimers mice reveals inflammation and dysfunction. Neurobiol. Aging 35, 2746-2760 (2014).
39. Mosher, K. I. & Wyss-Coray, T. Microglial dysfunction in brain aging and Alzheimers disease. Biochem. Pharmacol. 88, 594-604 (2014).
40. Heneka, M. T., OBanion, M. K., Terwel, D. & Kummer, M. P. Neuroinflammatory processes in Alzheimers disease. J. Neural Transm. Vienna Austria 1996 117, 919-947 (2010).
41. De Jong, E. K. et al. Expression of CXCL4 in microglia in vitro and in vivo and its possible signaling through CXCR3. J. Neurochem. 105, 1726-1736 (2008).
42. De Haas, A. H., Boddeke, H. W. G. M., Brouwer, N. & Biber, K. Optimized isolation enables ex vivo analysis of microglia from various central nervous system regions. Glia 55, 1374-1384 (2007).
43. De Haas, A. H., Boddeke, H. W. G. M. & Biber, K. Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 56, 888-894 (2008).
44. Van Weering, H. R. J. et al. CXCL10/CXCR3 signaling in glia cells differentially affects NMDA-induced cell death in CA and DG neurons of the mouse hippocampus. Hippocampus 21, 220-232 (2011).
45. Sun, A., Nguyen, X. V. & Bing, G. Comparative analysis of an improved thioflavin-s stain, Gallyas silver stain, and immunohistochemistry for neurofibrillary tangle demonstration on the same sections. J. Histochem. Cytochem. Off. J. Histochem. Soc. 50, 463-472 (2002).