Soluble phospho-tau from Alzheimer’s disease hippocampus drives microglial degeneration

Acta Neuropathologica

Volumn 132, Issue 6, 2016, Pages 897-916

  Sanchez Mejias, Elisabeth ^a,d   Navarro, Victoria ^b,c,d   Jimenez, Sebastian ^b,c,d   Sanchez Mico, Maria ^b,c,d   Sanchez Varo, Raquel ^a,d   Nuñez Diaz, Cristina ^a,d   Trujillo Estrada, Laura ^a,d   Davila, Jose Carlos ^a,d   Vizuete, Marisa ^b,c,d   Gutierrez, Antonia ^a,d   Vitorica, Javier ^b,c,d  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Alzheimer; Hippocampus; Human brain; Microglia; Pathology

Indexed keywords

AMYLOID PRECURSOR PROTEIN; TAU PROTEIN; AIF1 PROTEIN, HUMAN; CD45 ANTIGEN; CD68 ANTIGEN, HUMAN; DIFFERENTIATION ANTIGEN; DNA BINDING PROTEIN; LEUKOCYTE ANTIGEN; P2RY12 PROTEIN, HUMAN; PRESENILIN 1; PURINERGIC P2Y12 RECEPTOR;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DENSITY; DENTATE GYRUS; DISEASE COURSE; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOLOGICAL PARAMETERS; IN VITRO STUDY; MALE; MICROGLIA; MIDDLE AGED; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PARAHIPPOCAMPAL GYRUS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; CELL CULTURE; DIAGNOSTIC IMAGING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIGENS, CD; ANTIGENS, CD45; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; APOPTOSIS; CELLS, CULTURED; DISEASE PROGRESSION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MIDDLE AGED; PRESENILIN-1; RECEPTORS, PURINERGIC P2Y12; TAU PROTEINS;

EID: 84991092520     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-016-1630-5     Document Type: Article

References (66)

1. Asai H, Ikezu S, Tsunoda S, Medalla M, Luebke J, Haydar T, Wolozin B, Butovsky O, Kugler S, Ikezu T (2015) Depletion of microglia and inhibition of exosome synthesis halt tau propagation. Nat Neurosci 18:1584–1593
2. Bakker A, Krauss G, Albert M, Speck C, Jones L, Stark C, Yassa M, Bassett S, Shelton A, Gallagher M (2012) Reduction of hippocampal hyperactivity improves cognition in amnesic mild cognitive impairment. Neuron 74:467–474
3. Baron R, Babcock AA, Nemirovsky A, Finsen B, Monsonego A (2014) Accelerated microglial pathology is associated with Abeta plaques in mouse models of Alzheimer’s disease. Aging Cell 13:584–595
4. Braak H, Del Tredici K (2015) The preclinical phase of the pathological process underlying sporadic Alzheimer’s disease. Brain 138:2814–2833
5. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-[beta]-dependent molecular and functional signature in microglia. Nat Neurosci 17:131–143
6. Chitu V, Gokhan S, Nandi S, Mehler MF, Stanley ER (2016) Emerging roles for CSF-1 receptor and its ligands in the nervous system. Trends Neurosci 39:378–393
7. Condello C, Yuan P, Schain A, Grutzendler J (2015) Microglia constitute a barrier that prevents neurotoxic protofibrillar Aβ42 hotspots around plaques. Nat Commun 6:6176
8. Delobel P, Flament S, Hamdane M, Mailliot C, Sambo AV, Begard S, Sergeant N, Delacourte A, Vilain JP, Buee L (2002) Abnormal Tau phosphorylation of the Alzheimer-type also occurs during mitosis. J Neurochem 83:412–420
9. Fa M, Puzzo D, Piacentini R, Staniszewski A, Zhang H, Baltrons MA, Li Puma DD, Chatterjee I, Li J, Saeed F, Berman HL, Ripoli C, Gulisano W, Gonzalez J, Tian H, Costa JA, Lopez P, Davidowitz E, Yu WH, Haroutunian V, Brown LM, Palmeri A, Sigurdsson EM, Duff KE, Teich AF, Honig LS, Sierks M, Moe JG, D’Adamio L, Grassi C, Kanaan NM, Fraser PE, Arancio O (2016) Extracellular tau oligomers produce an immediate impairment of LTP and memory. Scientific Rep 6:19393
10. Fontaine SN, Zheng D, Sabbagh JJ, Martin MD, Chaput D, Darling A, Trotter JH, Stothert AR, Nordhues BA, Lussier A, Baker J, Shelton L, Kahn M, Blair LJ, Stevens SM Jr, Dickey CA (2016) DnaJ/Hsc70 chaperone complexes control the extracellular release of neurodegenerative-associated proteins. EMBO J 35:1537–1549
11. Frenkel D, Wilkinson K, Zhao L, Hickman SE, Means TK, Puckett L, Farfara D, Kingery ND, Weiner HL, El Khoury J (2013) Scara1 deficiency impairs clearance of soluble amyloid-beta by mononuclear phagocytes and accelerates Alzheimer’s-like disease progression. Nat Commun 4:2030
12. Fricker M, MaJ Oliva-Martin, Brown GC (2012) Primary phagocytosis of viable neurons by microglia activated with LPS or Abeta is dependent on calreticulin/LRP phagocytic signalling. J Neuroinflammation 9:1–12
13. Gomez-Nicola D, Perry VH (2015) Microglial dynamics and role in the healthy and diseased brain: a paradigm of functional plasticity. Neuroscientist 21:169–184
14. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JSK, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert JC, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, George-Hyslop P, Singleton A, Hardy J (2012) TREM2 variants in Alzheimer’s disease. N Engl J Med 368:117–127
15. Hamelin L, Lagarde J, Dorothee G, Leroy C, Labit M, Comley RA, de Souza LC, Corne H, Dauphinot L, Bertoux M, Dubois B, Gervais P, Colliot O, Potier MC, Bottlaender M, Sarazin M (2016) Early and protective microglial activation in Alzheimer’s disease: a prospective study using 18F-DPA-714 PET imaging. Brain 139:1252–1264
16. Heneka MT, Carson MJ, Khoury JE, Landreth GE, Brosseron F, Feinstein DL, Jacobs AH, Wyss-Coray T, Vitorica J, Ransohoff RM, Herrup K, Frautschy SA, Finsen B, Brown GC, Verkhratsky A, Yamanaka K, Koistinaho J, Latz E, Halle A, Petzold GC, Town T, Morgan D, Shinohara ML, Perry VH, Holmes C, Bazan NG, Brooks DJ, Sp Hunot, Joseph B, Deigendesch N, Garaschuk O, Boddeke E, Dinarello CA, Breitner JC, Cole GM, Golenbock DT, Kummer MP (2015) Neuroinflammation in Alzheimer’s disease. Lancet Neurol 14:388–405
17. Heneka MT, Kummer MP, Latz E (2014) Innate immune activation in neurodegenerative disease. Nat Rev Immunol 14:463–477
18. Heneka MT, O’Banion MK (2007) Inflammatory processes in Alzheimer’s disease. J Neuroimmunol 184:69–91
19. Heppner FL, Ransohoff RM, Becher B (2015) Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci 16:358–372
20. Hickman SE, Allison EK, El Khoury J (2008) Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer’s disease mice. J Neurosci 28:8354–8360
21. Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, Merry KM, Shi Q, Rosenthal A, Barres BA, Lemere CA, Selkoe DJ, Stevens B (2016) Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science 352:712–716
22. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J (2008) Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer’s disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 28:11650–11661
23. Jimenez S, Navarro V, Moyano J, Sanchez-Mico M, Torres M, Davila JC, Vizuete M, Gutierrez A, Vitorica J (2014) Disruption of amyloid plaques integrity affects the soluble oligomers content from Alzheimer disease brains. PLoS One 9:e114041
24. Jun G, Naj AC, Beecham GW (2010) MEta-analysis confirms cr1, clu, and picalm as alzheimer disease risk loci and reveals interactions with apoe genotypes. Arch Neurol 67:1473–1484
25. Kabir J, Lobo M, Zachary I (2002) Staurosporine induces endothelial cell apoptosis via focal adhesion kinase dephosphorylation and focal adhesion disassembly independent of focal adhesion kinase proteolysis. Biochem J 367:145–155
26. Korvatska O, Leverenz JB, Jayadev S (2015) R47 h variant of TREM2 associated with alzheimer disease in a large late-onset family: clinical, genetic, and neuropathological study. JAMA Neurol 72:920–927
27. Krauthausen M, Kummer MP, Zimmermann J, Reyes-Irisarri E, Terwel D, Bulic B, Heneka MT, Muller M (2015) CXCR3 promotes plaque formation and behavioral deficits in an Alzheimer’s disease model. J Clin Invest 125(1):365–378. doi:10.1172/JCI66771
28. Ksiezak-Reding H, Morgan K, Mattiace LA, Davies P, Liu WK, Yen SH, Weidenheim K, Dickson DW (1994) Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration. Am J Pathol 145:1496–1508
29. Luo W, Liu W, Hu X, Hanna M, Caravaca A, Paul SM (2015) Microglial internalization and degradation of pathological tau is enhanced by an anti-tau monoclonal antibody. Sci Rep 5:11161
30. Mai JK, Paxinos G, Voss T (2008) The human brain atlas. Academic Press, New York, USA
31. Maphis N, Xu G, Kokiko-Cochran ON, Cardona AE, Ransohoff RM, Lamb BT, Bhaskar K (2015) Loss of tau rescues inflammation-mediated neurodegeneration. Fron Neurosci 9:196
32. Maphis N, Xu G, Kokiko-Cochran ON, Jiang S, Cardona A, Ransohoff RM, Lamb BT, Bhaskar K (2015) Reactive microglia drive tau pathology and contribute to the spreading of pathological tau in the brain. Brain 138:1738–1755
33. Meyer-Luehmann M, Prinz M (2015) Myeloid cells in Alzheimer’s disease: culprits, victims or innocent bystanders? Trends Neurosci 38:659–668
34. Napoli I, Neumann H (2009) Microglial clearance function in health and disease. Neuroscience 158:1030–1038
35. Neumann H, Kotter MR, Franklin RJM (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132:288–295
36. Olmos-Alonso A, Schetters STT, Sri S, Askew K, Mancuso R, Vargas-Caballero M, Holscher C, Perry VH, Gomez-Nicola D (2016) Pharmacological targeting of CSF1R inhibits microglial proliferation and prevents the progression of Alzheimer’s-like pathology. Brain 139:891–907
37. Painter MM, Atagi Y, Liu CC, Rademakers R, Xu H, Fryer JD, Bu G (2015) TREM2 in CNS homeostasis and neurodegenerative disease. Mol Neurodegener 10:1–10
38. Paloneva J, Kestila M, Wu J, Salminen A, Bohling T, Ruotsalainen V, Hakola P, Bakker ABH, Phillips JH, Pekkarinen P, Lanier LL, Timonen T, Peltonen L (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25:357–361
39. Paloneva J, Manninen T, Christman G, Hovanes K, Mandelin J, Adolfsson R, Bianchin M, Bird T, Miranda R, Salmaggi A, Tranebjaerg L, Konttinen Y, Peltonen L (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71:656–662
40. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer’s disease. Neuron 55:697–711
41. Parkhurst C, Yang G, Ninan I, Savas J, Yates J III, Lafaille J, Hempstead B, Littman D, Gan WB (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609
42. Poliani PL, Wang Y, Fontana E, Robinette ML, Yamanishi Y, Gilfillan S, Colonna M (2015) TREM2 sustains microglial expansion during aging and response to demyelination. J Clin Invest 125:2161–2170
43. Ramos B, Baglietto-Vargas D, Rio JC, Moreno-Gonzalez I, Santa-Maria C, Jimenez S, Caballero C, Lopez-Tellez JF, Khan ZU, Ruano D, Gutierrez A, Vitorica J (2006) Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1/APP transgenic model of Alzheimer’s disease. Neurobiol Aging 27:1658–1672
44. Ransohoff RM, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119–145
45. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L (2007) Reducing endogenous tau ameliorates amyloid -induced deficits in an Alzheimer’s disease mouse model. Science 316:750
46. SantaCruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, Forster C, Yue M, Orne J, Janus C, Mariash A, Kuskowski M, Hyman B, Hutton M, Ashe KH (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309:476–481
47. Sastre M, Richardson JC, Gentleman SM (2011) Inflammatory risk factors and pathologies associated with Alzheimer’s disease. Curr Alzheimer Res 8:132–141
48. Schindowski K, Bretteville A, Leroy K, Begard SS, Brion JP, Hamdane M, Buee L (2006) Alzheimer’s disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am J Pathol 169:599–616
49. Serrano-Pozo A, Betensky RA, Frosch MP, Hyman BT (2016) Plaque-associated local toxicity increases over the clinical course of Alzheimer disease. Am J Pathol 186:375–384
50. Serrano-Pozo A, Gomez-Isla T, Growdon JH, Frosch MP, Hyman BT (2013) A phenotypic change but not proliferation underlies glial responses in Alzheimer disease. Am J Pathol 182:2332–2344
51. Serrano-Pozo A, Mielke ML, Gomez-Isla T, Betensky RA, Growdon JH, Frosch MP, Hyman BT (2011) Reactive glia not only associates with plaques but also parallels tangles in Alzheimer’s disease. Am J Pathol 179:1373–1384
52. Sierra A, Encinas JM, Deudero JJP, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483–495
53. Spangenberg EE, Lee RJ, Najafi AR, Rice RA, West BL, Green KN (2016) Eliminating microglia in Alzheimer’s mice prevents neuronal loss without modulating amyloid-β pathology. Brain 139:1265–1281
54. Streit WJ, Braak H, Xue QS, Bechmann I (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer’s disease. Acta Neuropathol 118:475–485
55. Tai HC, Serrano-Pozo A, Hashimoto T, Frosch MP, Spires-Jones TL, Hyman BT (2012) The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am J Pathol 181:1426–1435
56. Takeda S, Wegmann S, Cho H, DeVos SL, Commins C, Roe AD, Nicholls SB, Carlson GA, Pitstick R, Nobuhara CK, Costantino I, Frosch MP, Muller DJ, Irimia D, Hyman BT (2015) Neuronal uptake and propagation of a rare phosphorylated high-molecular-weight tau derived from Alzheimer/’s disease brain. Nat Commun 6:8490
57. Tischer J, Krueger M, Mueller W, Staszewski O, Prinz M, Streit WJ, Bechmann I (2016) Inhomogeneous distribution of Iba-1 characterizes microglial pathology in Alzheimer’s disease. Glia 64:1562–1572
58. Torres M, Jimenez S, Sanchez-Varo R, Navarro V, Trujillo-Estrada L, Sanchez-Mejias E, Carmona I, Davila JC, Vizuete M, Gutierrez A, Vitorica J (2012) Defective lysosomal proteolysis and axonal transport are early pathogenic events that worsen with age leading to increased APP metabolism and synaptic Abeta in transgenic APP/PS1 hippocampus. Mol Neurodegener 7:1–15
59. Ulland TK, Wang Y, Colonna M (2015) Regulation of microglial survival and proliferation in health and diseases. Semin Immunol 27:410–415
60. Verret L, Mann E, Hang G, Barth A, Cobos I, Ho K, Devidze N, Masliah E, Kreitzer A, Mody I, Mucke L, Palop J (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149:708–721
61. Vetrivel KS, Cheng H, Kim SH, Chen Y, Barnes NY, AlT Parent, Sisodia SS, Thinakaran G (2005) Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J Biol Chem 280:25892–25900
62. Wang X, Zhao L, Zhang J, Fariss RN, Ma W, Kretschmer F, Wang M, Qian Hh, Badea TC, Diamond JS, Gan WB, Roger JE, Wong WT (2016) Requirement for microglia for the maintenance of synaptic function and integrity in the mature retina. J Neurosci 36:2827–2842
63. Wang Y, Cella M, Mallinson K, Ulrich J, Young K, Robinette M, Gilfillan S, Krishnan G, Sudhakar S, Zinselmeyer B, Holtzman D, Cirrito J, Colonna M (2015) TREM2 lipid sensing sustains the microglial response in an Alzheimer’s disease model. Cell 160:1061–1071
64. Yamanaka M, Ishikawa T, Griep A, Axt D, Kummer MP, Heneka MT (2012) PPARgamma/RXRalpha-induced and CD36-mediated microglial amyloid-beta phagocytosis results in cognitive improvement in amyloid precursor protein/presenilin 1 mice. J Neurosci 32:17321–17331
65. Yeh F, Wang Y, Tom I, Gonzalez L, Sheng M (2016) TREM2 binds to apolipoproteins, including APOE and CLU/APOJ, and thereby facilitates uptake of amyloid-beta by microglia. Neuron 91(2):328–340. doi:10.1016/j.neuron.2016.06.015
66. Yuan P, Condello C, Keene C, Wang Y, Bird T, Paul S, Luo W, Colonna M, Baddeley D, Grutzendler J (2016) TREM2 haplodeficiency in mice and humans impairs the microglia barrier function leading to decreased amyloid compaction and severe axonal dystrophy. Neuron 90:724–739