Il10 deficiency rebalances innate immunity to mitigate Alzheimer-like pathology

Neuron

Volumn 85, Issue 3, 2015, Pages 534-548

  Guillot Sestier, Marie Victoire ^a   Doty, Kevin R ^a   Gate, David ^a   Rodriguez, Javier ^a   Leung, Brian P ^a   Rezai Zadeh, Kavon ^b   Town, Terrence ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; INTERLEUKIN 10; STAT3 PROTEIN; IL10 PROTEIN, HUMAN;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; CEREBRAL AMYLOIDOSIS; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE GENE; INHIBITION KINETICS; INNATE IMMUNITY; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NONHUMAN; PHAGOCYTOSIS; PROTEIN TRANSPORT; RNA SEQUENCE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; VERY ELDERLY; ANIMAL; C57BL MOUSE; DEFICIENCY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; FEMALE; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC;

EID: 84922026428     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.12.068     Document Type: Article

References (78)

1. Aguzzi A., Barres B.A., Bennett M.L. Microglia: scapegoat, saboteur, or something else?. Science 2013, 339:156-161.
2. Ahmed Z., Shaw G., Sharma V.P., Yang C., McGowan E., Dickson D.W. Actin-binding proteins coronin-1a and IBA-1 are effective microglial markers for immunohistochemistry. J.Histochem. Cytochem. 2007, 55:687-700.
3. Angelopoulos P., Agouridaki H., Vaiopoulos H., Siskou E., Doutsou K., Costa V., Baloyiannis S.I. Cytokines in Alzheimer's disease and vascular dementia. Int. J. Neurosci. 2008, 118:1659-1672.
4. Apelt J., Schliebs R. Beta-amyloid-induced glial expression of both pro- and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Res. 2001, 894:21-30.
5. Arosio B., Trabattoni D., Galimberti L., Bucciarelli P., Fasano F., Calabresi C., Cazzullo C.L., Vergani C., Annoni G., Clerici M. Interleukin-10 and interleukin-6 gene polymorphisms as risk factors for Alzheimer's disease. Neurobiol. Aging 2004, 25:1009-1015.
6. Bard F., Cannon C., Barbour R., Burke R.L., Games D., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., et al. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 2000, 6:916-919.
7. Brouwers N., Van Cauwenberghe C., Engelborghs S., Lambert J.C., Bettens K., Le Bastard N., Pasquier F., Montoya A.G., Peeters K., Mattheijssens M., et al. Alzheimer risk associated with a copy number variation in the complement receptor 1 increasing C3b/C4b binding sites. Mol. Psychiatry 2012, 17:223-233.
8. Butovsky O., Jedrychowski M.P., Moore C.S., Cialic R., Lanser A.J., Gabriely G., Koeglsperger T., Dake B., Wu P.M., Doykan C.E., et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 2014, 17:131-143.
9. Buttini M., Masliah E., Barbour R., Grajeda H., Motter R., Johnson-Wood K., Khan K., Seubert P., Freedman S., Schenk D., Games D. Beta-amyloid immunotherapy prevents synaptic degeneration in a mouse model of Alzheimer's disease. J.Neurosci. 2005, 25:9096-9101.
10. Chakrabarty P., Ceballos-Diaz C., Beccard A., Janus C., Dickson D., Golde T.E., Das P. IFN-gamma promotes complement expression andattenuates amyloid plaque deposition in amyloid beta precursor protein transgenic mice. J.Immunol. 2010, 184:5333-5343.
11. Chakrabarty P., Jansen-West K., Beccard A., Ceballos-Diaz C., Levites Y., Verbeeck C., Zubair A.C., Dickson D., Golde T.E., Das P. Massive gliosis induced by interleukin-6 suppresses Abeta deposition invivo: evidence against inflammation as a driving force for amyloid deposition. FASEB J. 2010, 24:548-559.
12. Chakrabarty P., Herring A., Ceballos-Diaz C., Das P., Golde T.E. Hippocampal expression of murine TNFα results in attenuation of amyloid deposition invivo. Mol. Neurodegener. 2011, 6:16.
13. Chakrabarty P., Li A., Ceballos-Diaz C., Eddy J.A., Funk C.C., Moore B., DiNunno N., Rosario A.M., Cruz P.E., Verbeeck C., et al. IL-10 Alters Immunoproteostasis in APP mice, Increasing Plaque Burden and Worsening Cognitive Behavior. Neuron 2015, 85:519-533. this issue.
14. Culpan D., Prince J.A., Matthews S., Palmer L., Hughes A., Love S., Kehoe P.G., Wilcock G.K. Neither sequence variation in the IL-10 gene promoter nor presence of IL-10 protein in the cerebral cortex is associated with Alzheimer's disease. Neurosci. Lett. 2006, 408:141-145.
15. de Hoon M.J., Imoto S., Nolan J., Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454.
16. De Strooper B., Iwatsubo T., Wolfe M.S. Presenilins and γ-secretase: structure, function, and role in Alzheimer Disease. Cold Spring Harb Perspect Med 2012, 2:a006304.
17. Deacon R.M., Bannerman D.M., Kirby B.P., Croucher A., Rawlins J.N. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav. Brain Res. 2002, 133:57-68.
18. Depboylu C., Du Y., Müller U., Kurz A., Zimmer R., Riemenschneider M., Gasser T., Oertel W.H., Klockgether T., Dodel R.C. Lack of association of interleukin-10 promoter region polymorphisms with Alzheimer's disease. Neurosci. Lett. 2003, 342:132-134.
19. Ellis R.J., Olichney J.M., Thal L.J., Mirra S.S., Morris J.C., Beekly D., Heyman A. Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: the CERAD experience, Part XV. Neurology 1996, 46:1592-1596.
20. Gandy S., Heppner F.L. Microglia as dynamic and essential components of the amyloid hypothesis. Neuron 2013, 78:575-577.
21. Ghassabeh G.H., De Baetselier P., Brys L., Noël W., Van Ginderachter J.A., Meerschaut S., Beschin A., Brombacher F., Raes G. Identification of a common gene signature for type II cytokine-associated myeloid cells elicited invivo in different pathologic conditions. Blood 2006, 108:575-583.
22. Grathwohl S.A., Kälin R.E., Bolmont T., Prokop S., Winkelmann G., Kaeser S.A., Odenthal J., Radde R., Eldh T., Gandy S., et al. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat. Neurosci. 2009, 12:1361-1363.
23. Guillot-Sestier M.V., Town T. Innate immunity in Alzheimer's disease: a complex affair. CNS Neurol. Disord. Drug Targets 2013, 12:593-607.
24. Hammond R.S., Tull L.E., Stackman R.W. On the delay-dependentinvolvement of the hippocampus in object recognition memory. Neurobiol. Learn. Mem. 2004, 82:26-34.
25. Herber D.L., Roth L.M., Wilson D., Wilson N., Mason J.E., Morgan D., Gordon M.N. Time-dependent reduction in Abeta levels after intracranial LPS administration in APP transgenic mice. Exp. Neurol. 2004, 190:245-253.
26. Hooijmans C.R., Van der Zee C.E., Dederen P.J., Brouwer K.M., Reijmer Y.D., van Groen T., Broersen L.M., Lütjohann D., Heerschap A., Kiliaan A.J. DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol. Dis. 2009, 33:482-498.
27. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
28. Imbimbo B.P., Giardino L., Sivilia S., Giuliani A., Gusciglio M., Pietrini V., Del Giudice E., D'Arrigo A., Leon A., Villetti G., Calzà L. CHF5074, a novel gamma-secretase modulator, restores hippocampal neurogenesis potential and reverses contextual memory deficit in a transgenic mouse model of Alzheimer's disease. J.Alzheimers Dis. 2010, 20:159-173.
29. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 2001, 17:157-165.
30. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., Copeland N.G., Lee M.K., Younkin L.H., Wagner S.L., et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloidpeptide invivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 2004, 13:159-170.
31. Kanekiyo T., Liu C.C., Shinohara M., Li J., Bu G. LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer's amyloid-β. J.Neurosci. 2012, 32:16458-16465.
32. Korotzer A.R., Pike C.J., Cotman C.W. beta-Amyloid peptides induce degeneration of cultured rat microglia. Brain Res. 1993, 624:121-125.
33. Krabbe G., Halle A., Matyash V., Rinnenthal J.L., Eom G.D., Bernhardt U., Miller K.R., Prokop S., Kettenmann H., Heppner F.L. Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology. PLoS ONE 2013, 8:e60921.
34. Kühn R., Löhler J., Rennick D., Rajewsky K., Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75:263-274.
35. Ledeboer A., Brevé J.J., Wierinckx A., van der Jagt S., Bristow A.F., Leysen J.E., Tilders F.J., Van Dam A.M. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur. J. Neurosci. 2002, 16:1175-1185.
36. Li M.O., Flavell R.A. Contextual regulation of inflammation: a duet by transforming growth factor-beta and interleukin-10. Immunity 2008, 28:468-476.
37. Lio D., Licastro F., Scola L., Chiappelli M., Grimaldi L.M., Crivello A., Colonna-Romano G., Candore G., Franceschi C., Caruso C. Interleukin-10 promoter polymorphism in sporadic Alzheimer's disease. Genes Immun. 2003, 4:234-238.
38. Loewenbrueck K.F., Tigno-Aranjuez J.T., Boehm B.O., Lehmann P.V., Tary-Lehmann M. Th1 responses to beta-amyloid in young humans convert to regulatory IL-10 responses in Down syndrome and Alzheimer's disease. Neurobiol. Aging 2010, 31:1732-1742.
39. Lopes K.O., Sparks D.L., Streit W.J. Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 2008, 56:1048-1060.
40. Ma S.L., Tang N.L., Lam L.C., Chiu H.F. The association between promoter polymorphism of the interleukin-10 gene and Alzheimer's disease. Neurobiol. Aging 2005, 26:1005-1010.
41. Maezawa I., Zimin P.I., Wulff H., Jin L.W. Amyloid-beta protein oligomer at low nanomolar concentrations activates microglia and induces microglial neurotoxicity. J.Biol. Chem. 2011, 286:3693-3706.
42. Mawuenyega K.G., Sigurdson W., Ovod V., Munsell L., Kasten T., Morris J.C., Yarasheski K.E., Bateman R.J. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2010, 330:1774.
43. McGeer P.L., Akiyama H., Itagaki S., McGeer E.G. Activation of the classical complement pathway in brain tissue of Alzheimer patients. Neurosci. Lett. 1989, 107:341-346.
44. Meda L., Cassatella M.A., Szendrei G.I., Otvos L., Baron P., Villalba M., Ferrari D., Rossi F. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 1995, 374:647-650.
45. Michelucci A., Heurtaux T., Grandbarbe L., Morga E., Heuschling P. Characterization of the microglial phenotype under specific pro-inflammatory and anti-inflammatory conditions: Effects of oligomeric and fibrillar amyloid-beta. J.Neuroimmunol. 2009, 210:3-12.
46. Miller K.R., Streit W.J. The effects of aging, injury and disease onmicroglial function: a case for cellular senescence. Neuron Glia Biol. 2007, 3:245-253.
47. Mucke L., Selkoe D.J. Neurotoxicity of amyloid β-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med 2012, 2:a006338.
48. Murray P.J. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 2006, 6:379-386.
49. Nicoll J.A., Wilkinson D., Holmes C., Steart P., Markham H., Weller R.O. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat. Med. 2003, 9:448-452.
50. Nicoll J.A., Barton E., Boche D., Neal J.W., Ferrer I., Thompson P., Vlachouli C., Wilkinson D., Bayer A., Games D., et al. Abeta species removal after abeta42 immunization. J.Neuropathol. Exp. Neurol. 2006, 65:1040-1048.
51. O'Leary T.P., Brown R.E. Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behav. Brain Res. 2009, 201:120-127.
52. Ramos E.M., Lin M.T., Larson E.B., Maezawa I., Tseng L.H., Edwards K.L., Schellenberg G.D., Hansen J.A., Kukull W.A., Jin L.W. Tumor necrosis factor alpha and interleukin 10 promoter region polymorphisms and risk of late-onset Alzheimer disease. Arch. Neurol. 2006, 63:1165-1169.
53. Richard K.L., Filali M., Préfontaine P., Rivest S. Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid beta 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J.Neurosci. 2008, 28:5784-5793.
54. Scassellati C., Zanardini R., Squitti R., Bocchio-Chiavetto L., Bonvicini C., Binetti G., Zanetti O., Cassetta E., Gennarelli M. Promoter haplotypes of interleukin-10 gene and sporadic Alzheimer's disease. Neurosci. Lett. 2004, 356:119-122.
55. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177.
56. Shaftel S.S., Kyrkanides S., Olschowka J.A., Miller J.N., Johnson R.E., O'Banion M.K. Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J.Clin. Invest. 2007, 117:1595-1604.
57. Sjölander J., Westermark G.T., Renström E., Blom A.M. Islet amyloid polypeptide triggers limited complement activation and binds complement inhibitor C4b-binding protein, which enhances fibril formation. J.Biol. Chem. 2012, 287:10824-10833.
58. Streit W.J., Braak H., Xue Q.S., Bechmann I. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathol. 2009, 118:475-485.
59. Strle K., Zhou J.H., Shen W.H., Broussard S.R., Johnson R.W., Freund G.G., Dantzer R., Kelley K.W. Interleukin-10 in the brain. Crit. Rev. Immunol. 2001, 21:427-449.
60. Tampellini D., Capetillo-Zarate E., Dumont M., Huang Z., Yu F., Lin M.T., Gouras G.K. Effects of synaptic modulation on beta-amyloid, synaptophysin, and memory performance in Alzheimer's disease transgenic mice. J.Neurosci. 2010, 30:14299-14304.
61. Tan J., Town T., Paris D., Mori T., Suo Z., Crawford F., Mattson M.P., Flavell R.A., Mullan M. Microglial activation resulting from CD40-CD40L interaction after beta-amyloid stimulation. Science 1999, 286:2352-2355.
62. Tan J., Town T., Mori T., Wu Y., Saxe M., Crawford F., Mullan M. CD45 opposes beta-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activated protein kinase. J.Neurosci. 2000, 20:7587-7594.
63. Tan J., Town T., Crawford F., Mori T., DelleDonne A., Crescentini R., Obregon D., Flavell R.A., Mullan M.J. Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat. Neurosci. 2002, 5:1288-1293.
64. Town T., Nikolic V., Tan J. The microglial "activation" continuum: from innate to adaptive responses. J.Neuroinflammation 2005, 2:24.
65. Town T., Laouar Y., Pittenger C., Mori T., Szekely C.A., Tan J., Duman R.S., Flavell R.A. Blocking TGF-beta-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat. Med. 2008, 14:681-687.
66. Townsend K.P., Town T., Mori T., Lue L.F., Shytle D., Sanberg P.R., Morgan D., Fernandez F., Flavell R.A., Tan J. CD40 signaling regulates innate and adaptive activation of microglia in response to amyloid beta-peptide. Eur. J. Immunol. 2005, 35:901-910.
67. Trouw L.A., Nielsen H.M., Minthon L., Londos E., Landberg G., Veerhuis R., Janciauskiene S., Blom A.M. C4b-binding protein in Alzheimer's disease: binding to Abeta1-42 and to dead cells. Mol. Immunol. 2008, 45:3649-3660.
68. Ubhi K., Peng K., Lessig S., Estrella J., Adame A., Galasko D., Salmon D.P., Hansen L.A., Kawas C.H., Masliah E. Neuropathology of dementia with Lewy bodies in advanced age: a comparison with Alzheimer disease. Neurosci. Lett. 2010, 485:222-227.
69. Vural P., Değirmencioğlu S., Parildar-Karpuzoğlu H., Doğru-Abbasoğlu S., Hanagasi H.A., Karadağ B., Gürvit H., Emre M., Uysal M. The combinations of TNFalpha-308 and IL-6 -174 or IL-10 -1082 genes polymorphisms suggest an association with susceptibility to sporadic late-onset Alzheimer's disease. Acta Neurol. Scand. 2009, 120:396-401.
70. Webster S.J., Bachstetter A.D., Van Eldik L.J. Comprehensive behavioral characterization of an APP/PS-1 double knock-in mouse model of Alzheimer's disease. Alzheimers Res Ther 2013, 5:28.
71. Weitz T.M., Town T. Microglia in Alzheimer's Disease: It's All About Context. Int. J. Alzheimers Dis. 2012, 2012:314185.
72. Wilcock D.M., Munireddy S.K., Rosenthal A., Ugen K.E., Gordon M.N., Morgan D. Microglial activation facilitates Abeta plaque removal following intracranial anti-Abeta antibody administration. Neurobiol. Dis. 2004, 15:11-20.
73. Williams L.M., Ricchetti G., Sarma U., Smallie T., Foxwell B.M. Interleukin-10 suppression of myeloid cell activation-a continuing puzzle. Immunology 2004, 113:281-292.
74. Wyss-Coray T., Mucke L. Inflammation in neurodegenerative disease-a double-edged sword. Neuron 2002, 35:419-432.
75. Wyss-Coray T., Lin C., Yan F., Yu G.Q., Rohde M., McConlogue L., Masliah E., Mucke L. TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat. Med. 2001, 7:612-618.
76. Zhang B., Gaiteri C., Bodea L.G., Wang Z., McElwee J., Podtelezhnikov A.A., Zhang C., Xie T., Tran L., Dobrin R., et al. Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 2013, 153:707-720.
77. Zhu Y., Hou H., Rezai-Zadeh K., Giunta B., Ruscin A., Gemma C., Jin J., Dragicevic N., Bradshaw P., Rasool S., et al. CD45 deficiency drives amyloid-β peptide oligomers and neuronal loss in Alzheimer's disease mice. J.Neurosci. 2011, 31:1355-1365.
78. Zotova E., Holmes C., Johnston D., Neal J.W., Nicoll J.A., Boche D. Microglial alterations in human Alzheimer's disease following Aβ42 immunization. Neuropathol. Appl. Neurobiol. 2011, 37:513-524.