Glial alterations from early to late stages in a model of Alzheimer's disease: Evidence of autophagy involvement in Aβ internalization

Hippocampus

Volumn 26, Issue 2, 2016, Pages 194-210

  Pomilio, Carlos ^a   Pavia, Patricio ^a   Gorojod, Roxana Mayra ^b   Vinuesa, Angeles ^a   Alaimo, Agustina ^b   Galvan, Veronica ^c   Kotler, Monica Lidia ^b   Beauquis, Juan ^a   Saravia, Flavia ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

AD; Astrocytes; Hilus; LC3; Microglia; Neuroinflammation; Stratum radiatum; Ubiquitin

Indexed keywords

AMYLOID BETA PROTEIN; CELL PROTEIN; CONGO RED; IBA1 PROTEIN; PROTEIN P62; UBIQUITIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHAGY; CELL DENSITY; CELL VOLUME; CONTROLLED STUDY; DENTATE GYRUS; DISEASE COURSE; GLIA; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; INTERNALIZATION; LIGHT CHAIN; MACROGLIA; MICROGLIA; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; RAT; SENESCENCE; STRATUM RADIATUM; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; AUTOPHAGY; CELL LINE, TUMOR; CELLS, CULTURED; DENTATE GYRUS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGLIA; RATS;

EID: 84956686151     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22503     Document Type: Article

References (62)

1. Abramoff MD, Magelhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophoton Int 11:36-42.
2. Bansal R, Staib LH, Laine AF, Hao X, Xu D, Liu J, Weissman M, Peterson BS. 2012. Anatomical brain images alone can accurately diagnose chronic neuropsychiatric illnesses. PLoS One 7:e50698.
3. Beauquis J, Roig P, Homo-Delarche F, De Nicola A, Saravia F. 2006. Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: Reversion by antidepressant treatment. Eur J Neurosci 23:1539-1546.
4. Beauquis J, Pavia P, Pomilio C, Vinuesa A, Podlutskaya N, Galvan V, Saravia F. 2013. Environmental enrichment prevents astroglial pathological changes in the hippocampus of APP transgenic mice, model of Alzheimer's disease. Exp Neurol 239:28-37.
5. Beauquis J, Vinuesa A, Pomilio C, Pavia P, Galvan V, Saravia F. 2014. Neuronal and glial alterations, increased anxiety, and cognitive impairment before hippocampal amyloid deposition in PDAPP mice, model of Alzheimer's disease. Hippocampus 24:257-269.
6. Benda P, Lightbody J, Sato G, Levine L, Sweet W. 1968. Differentiated rat glial cell strain in tissue culture. Science 161:370-371.
7. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603-614.
8. Blennow K, de Leon MJ, Zetterberg H. 2006. Alzheimer's disease. Lancet 368:387-403.
9. Cho MH, Cho K, Kang HJ, Jeon EY, Kim HS, Kwon HJ, Kim HM, Kim DH, Yoon SY. 2014. Autophagy in microglia degrades extracellular beta-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy 10:1761-1775.
10. Chvatal A, Anderova M, Hock M, Prajerova I, Neprasova H, Chvatal V, Kirchhoff F, Sykova E. 2007. Three-dimensional confocal morphometry reveals structural changes in astrocyte morphology in situ. J Neurosci Res 85:260-271.
11. Dantuma NP, Bott LC. 2014. The ubiquitin-proteasome system in neurodegenerative diseases: Precipitating factor, yet part of the solution. Front Mol Neurosci 7:70.
12. de Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. 1998. Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269-301.
13. Di Malta C, Fryer JD, Settembre C, Ballabio A. 2012. Astrocyte dysfunction triggers neurodegeneration in a lysosomal storage disorder. Proc Natl Acad Sci USA 109:E2334-E2342.
14. Dubois B, Feldman HH, Jacova C, Cummings JL, DeKosky ST, Barberger-Gateau P, Delacourte A, Frisoni G, Fox NC, Galasko D, et al. 2010. Revising the definition of Alzheimer's disease: A new lexicon. Lancet Neurol 9:1118-1127.
15. Ferrera D, Mazzaro N, Canale C, Gasparini L. 2014. Resting microglia react to Aβ42 fibrils but do not detect oligomers or oligomer-induced neuronal damage. Neurobiol Aging 2444-2457.
16. Francois A, Terro F, Janet T, Rioux BA, Paccalin M, Page G. 2013. Involvement of interleukin-1beta in the autophagic process of microglia: Relevance to Alzheimer's disease. J Neuroinflammation 10:151.
17. Fu Y, Rusznak Z, Kwok JB, Kim WS, Paxinos G. 2014. Age-dependent alterations of the hippocampal cell composition and proliferative potential in the hAbetaPPSwInd-J20 mouse. J Alzheimers Dis 41:1177-1192.
18. Galvan V, Gorostiza OF, Banwait S, Ataie M, Logvinova AV, Sitaraman S, Carlson E, Sagi SA, Chevallier N, Jin K, et al. 2006. Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc Natl Acad Sci USA 103:7130-7135.
19. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392-395.
20. Hefendehl JK, Neher JJ, Suhs RB, Kohsaka S, Skodras A, Jucker M. 2014. Homeostatic and injury-induced microglia behavior in the aging brain. Aging Cell 13:60-69.
21. Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, et al. 2013. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493:674-678.
22. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L. 1999. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
23. Jaeger PA, Wyss-Coray T. 2009. All-you-can-eat: Autophagy in neurodegeneration and neuroprotection. Mol Neurodegener 4:16.
24. Jansen AH, Reits EA, Hol EM. 2014. The ubiquitin proteasome system in glia and its role in neurodegenerative diseases. Front Mol Neurosci 7:73.
25. Kim HJ, Chae SC, Lee DK, Chromy B, Lee SC, Park YC, Klein WL, Krafft GA, Hong ST. 2003. Selective neuronal degeneration induced by soluble oligomeric amyloid beta protein. FASEB J 17:118-120.
26. Krabbe G, Halle A, Matyash V, Rinnenthal JL, Eom GD, Bernhardt U, Miller KR, Prokop S, Kettenmann H, Heppner FL. 2013. Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology. PLoS One 8:e60921.
27. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, Viola KL, Klein WL. 2007. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27:796-807.
28. Lin AL, Zheng W, Halloran JJ, Burbank RR, Hussong SA, Hart MJ, Javors M, Shih YY, Muir E, Solano FR, et al. 2013. Chronic rapamycin restores brain vascular integrity and function through NO synthase activation and improves memory in symptomatic mice modeling Alzheimer's disease. J Cereb Blood Flow Metab 33:1412-1421.
29. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J. 1999. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862.
30. Maia GH, Quesado JL, Soares JI, do Carmo JM, Andrade PA, Andrade JP, Lukoyanov NV. 2014. Loss of hippocampal neurons after kainate treatment correlates with behavioral deficits. PLoS One 9:e84722.
31. Majumder S, Richardson A, Strong R, Oddo S. 2011. Inducing autophagy by rapamycin before, but not after, the formation of plaques and tangles ameliorates cognitive deficits. PLoS One 6:e25416.
32. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE. 2009. Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29:4252-4262.
33. Marlatt MW, Lucassen PJ. 2010. Neurogenesis and Alzheimer's disease: Biology and pathophysiology in mice and men. Curr Alzheimer Res 7:113-125.
34. Martinez-Vicente M, Cuervo AM. 2007. Autophagy and neurodegeneration: When the cleaning crew goes on strike. Lancet Neurol 6:352-361.
35. Mizushima N, Sugita H, Yoshimori T, Ohsumi Y. 1998. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 273:33889-33892.
36. Mohamed A, Posse dC. 2011. Abeta internalization by neurons and glia. Int J Alzheimers Dis 2011:127984.
37. Montagne A, Barnes SR, Sweeney MD, Halliday MR, Sagare AP, Zhao Z, Toga AW, Jacobs RE, Liu CY, Amezcua L, et al. 2015. Blood-brain barrier breakdown in the aging human hippocampus. Neuron 85:296-302.
38. Mosher KI, Wyss-Coray T. 2014. Microglial dysfunction in brain aging and Alzheimer's disease. Biochem Pharmacol 88:594-604.
39. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
40. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L. 2000. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
41. Nagele RG, Wegiel J, Venkataraman V, Imaki H, Wang KC, Wegiel J. 2004. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol Aging 25:663-674.
42. Nielsen HM, Mulder SD, Belien JA, Musters RJ, Eikelenboom P, Veerhuis R. 2010. Astrocytic A beta 1-42 uptake is determined by A beta-aggregation state and the presence of amyloid-associated proteins. Glia 58:1235-1246.
43. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM. 2005. Extensive involvement of autophagy in Alzheimer disease: An immuno-electron microscopy study. J Neuropathol Exp Neurol 64:113-122.
44. Pihlaja R, Koistinaho J, Malm T, Sikkila H, Vainio S, Koistinaho M. 2008. Transplanted astrocytes internalize deposited beta-amyloid peptides in a transgenic mouse model of Alzheimer's disease. Glia 56:154-163.
45. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, et al. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36:585-595.
46. 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 beta-induced deficits in an Alzheimer's disease mouse model. Science 316:750-754.
47. Rodriguez JJ, Olabarria M, Chvatal A, Verkhratsky A. 2009. Astroglia in dementia and Alzheimer's disease. Cell Death Differ 16:378-385.
48. Santos RX, Correia SC, Cardoso S, Carvalho C, Santos MS, Moreira PI. 2011. Effects of rapamycin and TOR on aging and memory: Implications for Alzheimer's disease. J Neurochem 117:927-936.
49. Selkoe DJ. 2000. Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 924:17-25.
50. Sierra A, Abiega O, Shahraz A, Neumann H. 2013. Janus-faced microglia: Beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6.
51. Simón AM, Schiapparelli L, Salazar-Colocho P, Cuadrado-Tejedor M, Escribano L, López de Maturana R, Del Río J, Pérez-Mediavilla A, Frechilla D. 2008. Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to Abeta levels. Neurobiol Dis 2009;33:369-378.
52. Spiegel AM, Koh MT, Vogt NM, Rapp PR, Gallagher M. 2013. Hilar interneuron vulnerability distinguishes aged rats with memory impairment. J Comp Neurol 521:3508-3523.
53. Spilman P, Podlutskaya N, Hart MJ, Debnath J, Gorostiza O, Bredesen D, Richardson A, Strong R, Galvan V. 2010. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 5:e9979.
54. Steele ML, Robinson SR. 2012. Reactive astrocytes give neurons less support: Implications for Alzheimer's disease. Neurobiol Aging 33:423-413.
55. Takahashi H, Brasnjevic I, Rutten BP, Van Der KN, Perl DP, Bouras C, Steinbusch HW, Schmitz C, Hof PR, Dickstein DL. 2010. Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer's disease. Brain Struct Funct 214:145-160.
56. Verkhratsky A, Rodriguez JJ, Parpura V. 2014. Neuroglia in ageing and disease. Cell Tissue Res 357:493-503.
57. Verkhratsky A, Marutle A, Rodríguez-Arellano JJ, Nordberg A. 2014. Glial asthenia and functional paralysis: A new perspective on neurodegeneration and Alzheimer's disease. Neuroscientist 14 pii: 1073858414547132.
58. Whitney IE, Keeley PW, Raven MA, Reese BE. 2008. Spatial patterning of cholinergic amacrine cells in the mouse retina. J Comp Neurol 508:1-12.
59. Wilcock DM, Gordon MN, Morgan D. 2006. Quantification of cerebral amyloid angiopathy and parenchymal amyloid plaques with Congo red histochemical stain. Nat Protoc 1:1591-1595.
60. Wilkinson JE, Burmeister L, Brooks SV, Chan CC, Friedline S, Harrison DE, Hejtmancik JF, Nadon N, Strong R, Wood LK, et al. 2012. Rapamycin slows aging in mice. Aging Cell 11:675-682.
61. Wright AL, Zinn R, Hohensinn B, Konen LM, Beynon SB, Tan RP, Clark IA, Abdipranoto A, Vissel B. 2013. Neuroinflammation and neuronal loss precede Abeta plaque deposition in the hAPP-J20 mouse model of Alzheimer's disease. PLoS One 8:e59586.
62. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, Mohan PS, Mercken M, Farmery MR, Tjernberg LO, et al. 2005. Macroautophagy-A novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J Cell Biol 171:87-98.