Migration of blood cells to β-amyloid plaques in Alzheimer's disease

Experimental Gerontology

Volumn 65, Issue , 2015, Pages 8-15

  Hohsfield, Lindsay A ^a   Humpel, Christian ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; AMYLOID PLAQUE; BLOOD BRAIN BARRIER; BLOOD CELL; CELL FUNCTION; CELL INFILTRATION; CELL MIGRATION; CELL PHAGOCYTOSIS; ERYTHROCYTE; GRANULOCYTE; HUMAN; LEUKOCYTE; LYMPHOCYTE MIGRATION; MICROGLIA; MONOCYTE; NERVOUS SYSTEM INFLAMMATION; NEUROPHYSIOLOGICAL RECRUITMENT; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; THROMBOCYTE; BRAIN; CELL MOTION; METABOLISM; NEUROFIBRILLARY TANGLE; PATHOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; BLOOD CELLS; BRAIN; CELL MOVEMENT; HUMANS; NEUROFIBRILLARY TANGLES; PLAQUE, AMYLOID;

EID: 84924673435     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2015.03.002     Document Type: Review

References (99)

1. Akiyama H., Kondo H., Mori H., Kametani F., Nishimura T., Ikeda K., Kato M., McGeer P.L. The amino-terminally truncated forms of amyloid beta-protein in brain macrophages in the ischemic lesions of Alzheimer's disease patients. Neurosci. Lett. 1996, 219:115-118.
2. Akiyama H., Barger S., Barnum S., Bradt B., Bauer J., Cole G.M., Cooper N.R., Eikelenboom P., Emmerling M., Fiebich B.L., et al. Inflammation and Alzheimer's disease. Neurobiol. Aging 2000, 21:383-421.
3. Auffray C., Fogg D.K., Narni-Mancinelli E., Senechal B., Trouillet C., Saederup N., Leemput J., Bigot K., Campisi L., Abitbol M., et al. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 2009, 206:595-606.
4. Baik S.H., Cha M.Y., Hyun Y.M., Cho H., Hamza B., Kim D.K., Han S.H., Choi H., Kim K.H., Moon M., et al. Migration of neutrophils targeting amyloid plaques in Alzheimer's disease mouse model. Neurobiol. Aging 2014, 35:1286-1292.
5. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., Landreth G.E. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 2003, 23:2665-2674.
6. Blass J.P., Hanin I., Barclay L., Kopp U., Reding M.J. Red blood cell abnormalities in Alzheimer disease. J. Am. Geriatr. Soc. 1985, 33:401-405.
7. Boissonneault V., Filali M., Lessard M., Relton J., Wong G., Rivest S. Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 2009, 132:1078-1092.
8. Britschgi M., Wyss-Coray T. Immune cells may fend off Alzheimer disease. Nat. Med. 2007, 13:408-409.
9. Buckner C.M., Calderon T.M., Willams D.W., Belbin T.J., Berman J.W. Characterization of monocyte maturation/differentiation that facilitates their transmigration across the blood-brain barrier and infection by HIV: implications for NeuroAIDS. Cell. Immunol. 2011, 267:109-123.
10. Buckwalter M.S., Coleman B.S., Buttini M., Barbour R., Schenk D., Games D., Seubert P., Wyss-Coray T. Increased T cell recruitment to the CNS after amyloid beta 1-42 immunization in Alzheimer's mice overproducing transforming growth factor-beta 1. J. Neurosci. 2006, 26:11437-11441.
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 in vivo: evidence against inflammation as a driving force for amyloid deposition. FASEB J. 2010, 24:548-559.
12. Chen K., Liu M., Liu Y., Wang C., Yoshimura T., Gong W., Le Y., Tessarollo L., Wang J.M. Signal relay by CC chemokine receptor 2 (CCR2) and formylpeptide receptor 2 (Fpr2) in the recruitment of monocyte-derived dendritic cells in allergic airway inflammation. J. Biol. Chem. 2013, 288:16262-16273.
13. Combs C.K., Karlo J.C., Kao S.C., Landreth G.E. beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J. Neurosci. 2001, 21:1179-1188.
14. Coraci I.S., Husemann J., Berman J.W., Hulette C., Dufour J.H., Campanella G.K., Luster A.D., Silverstein S.C., El-Khoury J.B. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to beta-amyloid fibrils. Am. J. Pathol. 2002, 160:101-112.
15. Cortes-Canteli M., Zamolodchikov D., Ahn H.J., Strickland S., Norris E.H. Fibrinogen and altered hemostasis in Alzheimer's disease. J. Alzheimers Dis. 2012, 32:599-608.
16. El Khoury J., Luster A.D. Mechanisms of microglia accumulation in Alzheimer's disease: therapeutic implications. Trends Pharm. Sci. 2008, 29:626-632.
17. El Khoury J.B., Moore K.J., Means T.K., Leung J., Terada K., Toft M., Freeman M.W., Luster A.D. CD36 mediates the innate host response to beta-amyloid. J. Exp. Med. 2003, 197:1657-1666.
18. El Khoury J., Toft M., Hickman S.E., Means T.K., Terada K., Geula C., Luster A.D. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat. Med. 2007, 13:432-438.
19. Estes M.L., McAllister A.K. Alterations in immune cells and mediators in the brain: it's not always neuroinflammation!. Brain Pathol. 2014, 24:623-630. (Zurich, Switzerland).
20. Evin G., Zhu A.H.R., Masters C.L., Li Q.X. Proteolytic processing of the Alzheimer's disease amyloid precursor protein in brain and platelets. J. Neurosci. Res. 2003, 74:386-392.
21. Fiala M., Zhang L., Gan X., Sherry B., Taub D., Graves M.C., Hama S., Way D., Weinand M., Witte M., et al. Amyloid-beta induces chemokine secretion and monocyte migration across a human blood-brain barrier model. Mol. Med. 1998, 4:480-489.
22. Fiala M., Lin J., Ringman J., Kermani-Arab V., Tsao G., Patel A., Lossinsky A.S., Graves M.C., Gustavson A., Sayre J., Sofroni E., Suarez T., Chiappelli F., Bernard G. Ineffective phagocytosis of amyloid-beta by macrophages of Alzheimer's disease patients. J. Alzheimers Dis. 2005, 7:221-232.
23. Fiala M., Liu P.T., Espinosa-Jeffrey A., Rosenthal M.J., Bernard G., Ringman J.M., Sayre J., Zhang L., Zaghi J., Dejbakhsh S., et al. Innate immunity and transcription of MGAT-III and Toll-like receptors in Alzheimer's disease patients are improved by bisdemethoxycurcumin. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12849-12854.
24. Fisher Y., Nemirovsky A., Baron R., Monsonego A. T cells specifically targeted to amyloid plaques enhance plaque clearance in a mouse model of Alzheimer's disease. PLoS One 2010, 5:e10830.
25. Fisher Y., Strominger I., Biton S., Nemirovsky A., Baron R., Monsonego A. Th1 polarization of T cells injected into the cerebrospinal fluid induces brain immunosurveillance. J. Immunol. 2014, 192:92-102.
26. Frenkel D., Wilkinson K., Zhao L., Hickman S.E., Means T.K., Puckett L., Farfara D., Kingery N.D., Weiner H.L., El Khoury J. Scara1 deficiency impairs clearance of soluble amyloid-β by mononuclear phagocytes and accelerates Alzheimer's-like disease progression. Nat. Commun. 2013, 4:2030.
27. Gate D., Rezai-Zadeh K., Jodry D., Rentsendorj A., Town T. Macrophages in Alzheimer's disease: the blood-borne identity. J. Neural Transm. 2010, 117:961-970.
28. Giri R., Shen Y., Stins M., Du Yan S., Schmidt A.M., Stern D., Kim K.S., Zlokovic B., Kalra V.K. beta-Amyloid-induced migration of monocytes across human brain endothelial cells involves RAGE and PECAM-1. Am. J. Physiol. Cell Physiol. 2000, 279:C1772-1781.
29. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
30. Gordon S., Taylor P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005, 5:953-964.
31. Grathwohl S.A., Kalin 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.
32. Halle A., Hornung V., Petzold G.C., Stewart C.R., Monks B.G., Reinheckel T., Fitzgerald K.A., Latz E., Moore K.J., Golenbock D.T. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 2008, 9:857-865.
33. Hawkes C.A., McLaurin J. Selective targeting of perivascular macrophages for clearance of beta-amyloid in cerebral amyloid angiopathy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1261-1266.
34. Heneka M.T., Kummer M.P., Stutz A., Delekate A., Schwartz S., Vieira-Saecker A., Griep A., Axt D., Remus A., Tzeng T.C., Gelpi E., Halle A., Korte M., Latz E., Golenbock D.T. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 2013, 493:674-678.
35. Hickman S.E., El Khoury J. Mechanisms of mononuclear phagocyte recruitment in Alzheimer's disease. Curr. Drug Targets CNS Neurol. Disord. 2010, 9:168-173.
36. Hickman S.E., El Khoury J. TREM2 and the neuroimmunology of Alzheimer's disease. Biochem. Pharmacol. 2014, 88:495-498.
37. Hohsfield L.A., Ehrlich D., Humpel C. Intravenous infusion of nerve growth factor-secreting monocytes supports the survival of cholinergic neurons in the nucleus basalis of Meynert in hypercholesterolemia Brown-Norway rats. J. Neurosci. Res. 2014, 92:298-306.
38. Humpel C. Basolateral aggregated rat amyloid beta(1-42) potentiates transmigration of primary rat monocytes through a rat blood-brain barrier. Curr. Neurovasc. Res. 2008, 5:185-192.
39. Iribarren P., Zhou Y., Hu J., Le Y., Wang J. The role of formyl peptide receptor like 1 (FPRL1/MFPR2) in mononuclear phagocyte responses in Alzheimer's disease. Immunol. Res. 2005, 31:165-176.
40. Itagaki S., McGeer P.L., Akiyama H. Presence of T-cytotoxic suppressor and leucocyte common antigen positive cells in Alzheimer's disease brain tissue. Neurosci. Lett. 1988, 91:259-264.
41. Joslin G., Griffin G.L., August A.M., Adams S., Fallon R.J., Senior R.M., Perlmutter D.H. The serpin-enzyme complex (SEC) receptor mediates the neutrophil chemotactic effect of alpha-1 antitrypsin-elastase complexes and amyloid-beta peptide. J. Clin. Investig. 1992, 90:1150-1154.
42. Kaneider N.C., Lindner J., Feistritzer C., Sturn D.H., Mosheimer B.A., Djanani A.M., Wiedermann C.J. The immune modulator FTY720 targets sphingosine-kinase-dependent migration of human monocytes in response to amyloid beta-protein and its precursor. FASEB J. 2004, 18:1309-1311.
43. Khandelwal P.J., Herman A.M., Moussa C.E. Inflammation in the early stages of neurodegenerative pathology. J. Neuroimmunol. 2011, 238:1-11.
44. Kiyota T., Yamamoto M., Xiong H., Lambert M.P., Klein W.L., Gendelman H.E., Ransohoff R.M., Ikezu T. CCL2 accelerates microglia-mediated Abeta oligomer formation and progression of neurocognitive dysfunction. PLoS One 2009, 4:e6197.
45. Kniewallner K.M., Ehrlich D., Kiefer A., Marksteiner J., Humpel C. Platelets in the Alzheimer's disease brain: do they play a role in cerebral amyloid angiopathy?. Curr. Neurovasc. Res. 2015, (2015 Jan 2 [Epub ahead of print]).
46. Kumar-Singh S., Pirici D., McGowan E., Serneels S., Ceuterick C., Hardy J., Duff K., Dickson D., Van Broeckhoven C. Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am. J. Pathol. 2005, 167:527-543.
47. LaFerla F.M., Green K.N., Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat. Rev. Neurosci. 2007, 8:499-509.
48. Lampron A., Pimentel-Coelho P.M., Rivest S. Migration of bone marrow-derived cells into the central nervous system in models of neurodegeneration. J. Comp. Neurol. 2013, 521:3863-3876.
49. Larbi A., Pawelec G., Witkowski J.M., Schipper H.M., Derhovanessian E., Goldeck D., Fulop T. Dramatic shifts in circulating CD4 but not CD8 T cell subsets in mild Alzheimer's disease. J. Alzheimers Dis. 2009, 17:91-103.
50. Lebson L., Nash K., Kamath S., Herber D., Carty N., Lee D.C., Li Q., Szekeres K., Jinwal U., Koren J., et al. Trafficking CD11b-positive blood cells deliver therapeutic genes to the brain of amyloid-depositing transgenic mice. J. Neurosci. 2010, 30:9651-9658.
51. Li M., Shang D.S., Zhao W.D., Tian L., Li B., Fang W.G., Zhu L., Man S.M., Chen Y.H. Amyloid beta interaction with receptor for advanced glycation end products up-regulates brain endothelial CCR5 expression and promotes T cells crossing the blood-brain barrier. J. Immunol. 2009, 182:5778-5788.
52. Liu Y.J., Guo D.W., Tian L., Shang D.S., Zhao W.D., Li B., Fang W.G., Zhu L., Chen Y.H. Peripheral T cells derived from Alzheimer's disease patients overexpress CXCR2 contributing to its transendothelial migration, which is microglial TNF-alpha-dependent. Neurobiol. Aging 2010, 31:175-188.
53. Lucin K.M., Wyss-Coray T. Immune activation in brain aging and neurodegeneration: too much or too little?. Neuron 2009, 64:110-122.
54. Lynch M.A., Mills K.H. Immunology meets neuroscience-opportunities for immune intervention in neurodegenerative diseases. Brain Behav. Immun. 2012, 26:1-10.
55. Malm T.M., Koistinaho M., Parepalo M., Vatanen T., Ooka A., Karlsson S., Koistinaho J. Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol. Dis. 2005, 18:134-142.
56. Malm T., Koistinaho M., Muona A., Magga J., Koistinaho J. The role and therapeutic potential of monocytic cells in Alzheimer's disease. Glia 2010, 58:889-900.
57. Man S.M., Ma Y.R., Shang D.S., Zhao W.D., Li B., Guo D.W., Fang W.G., Zhu L., Chen Y.H. Peripheral T cells overexpress MIP-1alpha to enhance its transendothelial migration in Alzheimer's disease. Neurobiol. Aging 2007, 28:485-496.
58. Michaud J.P., Bellavance M.A., Prefontaine P., Rivest S. Real-time in vivo imaging reveals the ability of monocytes to clear vascular amyloid Beta. Cell Rep. 2013, 5:646-653.
59. Mildner A., Schlevogt B., Kierdorf K., Bottcher C., Erny D., Kummer M.P., Quinn M., Bruck W., Bechmann I., Heneka M.T., et al. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J. Neurosci. 2011, 31:11159-11171.
60. Mizwicki M.T., Liu G., Fiala M., Magpantay L., Sayre J., Siani A., Mahanian M., Weitzman R., Hayden E.Y., Rosenthal M.J., Nemere I., Ringman J., Teplow D.B. 1α,25-Dihydroxyvitamin D3 and resolvin D1 retune the balance between amyloid-β phagocytosis and inflammation in Alzheimer's disease patients. J. Alzheimers Dis. 2013, 34:155-170.
61. Mohanty J.G., Shukla H.D., Williamson J.D., Launer L.J., Saxena S., Rifkind J.M. Alterations in the red blood cell membrane proteome in Alzheimer's subjects reflect disease-related changes and provide insight into altered cell morphology. Proteome Sci. 2010, 8:11.
62. Monsonego A., Zota V., Karni A., Krieger J.I., Bar-Or A., Bitan G., Budson A.E., Sperling R., Selkoe D.J., Weiner H.L. Increased T cell reactivity to amyloid beta protein in older humans and patients with Alzheimer disease. J. Clin. Invest. 2003, 112:415-422.
63. Monsonego A., Imitola J., Petrovic S., Zota V., Nemirovsky A., Baron R., Fisher Y., Owens T., Weiner H.L. Abeta-induced meningoencephalitis is IFN-gamma-dependent and is associated with T cell-dependent clearance of Abeta in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5048-5053.
64. Monsonego A., Nemirovsky A., Harpaz I. CD4 T cells in immunity and immunotherapy of Alzheimer's disease. Immunology 2013, 139:438-446.
65. Mufson E.J., Counts S.E., Perez S.E., Ginsberg S.D. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert. Rev. Neurother. 2008, 8:1703-1718.
66. Naert G., Rivest S. A deficiency in CCR2+ monocytes: the hidden side of Alzheimer's disease. J. Mol. Cell Biol. 2013, 5:284-293.
67. Padovani A., Pastorino L., Borroni B., Colciaghi F., Rozzini L., Monastero R., Perez J., Pettenati C., Mussi M., Parrinello G., Cottini E., Lenzi L., Trabucchi M., Cattabeni F., Di Luca M. Amyloid precursor protein in platelets: a peripheral marker for the diagnosis of sporadic AD. Neurology 2001, 57:2243-2248.
68. Perl D.P. Neuropathology of Alzheimer's disease. Mt Sinai J. Med. New York 2010, 77:32-42.
69. Prinz M., Priller J., Sisodia S.S., Ransohoff R.M. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat. Neurosci. 2011, 14:1227-1235.
70. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
71. Ransohoff R.M., Brown M.A. Innate immunity in the central nervous system. J. Clin. Invest. 2012, 122:1164-1171.
72. Rezai-Zadeh K., Gate D., Town T. CNS infiltration of peripheral immune cells: D-Day for neurodegenerative disease?. J. NeuroImmune Pharm. 2009, 4:462-475.
73. Rogers J., Luber-Narod J., Styren S.D., Civin W.H. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol. Aging 1988, 9:339-349.
74. Rossi B., Angiari S., Zenaro E., Budui S.L., Constantin G. Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyte-endothelial interactions. J. Leukoc. Biol. 2011, 89:539-556.
75. Sabolovic D., Roudier M., Boynard M., Pautou C., Sestier C., Fertil B., Geldwerth D., Roger J., Pons J.N., Amri A., et al. Membrane modifications of red blood cells in Alzheimer's disease. J. Gerontol. A: Biol. Med. Sci. 1997, 52:B217-220.
76. Schwartz M., Shechter R. Systemic inflammatory cells fight off neurodegenerative disease. Nat. Rev. Neurol. 2010, 6:405-410.
77. Serrano-Pozo A., Frosch M.P., Masliah E., Hyman B.T. Neuropathological alterations in Alzheimer disease. Cold Spring Harbor Perspect. Med. 2011, 1:a006189.
78. Sheedy F.J., Grebe A., Rayner K.J., Kalantari P., Ramkhelawon B., Carpenter S.B., Becker C.E., Ediriweera H.N., Mullick A.E., Golenbock D.T., Stuart L.M., Latz E., Fitzgerald K.A., Moore K.J. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat. Immunol. 2013, 14:812-820.
79. Shi C., Pamer E.G. Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 2011, 11:762-774.
80. Simard A.R., Soulet D., Gowing G., Julien J.P., Rivest S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006, 49:489-502.
81. Sokolowski J.D., Mandell J.W. Phagocytic clearance in neurodegeneration. Am. J. Pathol. 2011, 178:1416-1428.
82. Stalder A.K., Ermini F., Bondolfi L., Krenger W., Burbach G.J., Deller T., Coomaraswamy J., Staufenbiel M., Landmann R., Jucker M. Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J. Neurosci. 2005, 25:11125-11132.
83. Strauss-Ayali D., Conrad S.M., Mosser D.M. Monocyte subpopulations and their differentiation patterns during infection. J. Leukoc. Biol. 2007, 82:244-252.
84. Tacke F., Randolph G.J. Migratory fate and differentiation of blood monocyte subsets. Immunobiology 2006, 211:609-618.
85. Thornton P., McColl B.W., Greenhalgh A., Denes A., Allan S.M., Rothwell N.J. Platelet interleukin-1alpha drives cerebrovascular inflammation. Blood 2010, 115:3632-3639.
86. Togo T., Akiyama H., Iseki E., Kondo H., Ikeda K., Kato M., Oda T., Tsuchiya K., Kosaka K. Occurrence of T cells in the brain of Alzheimer's disease and other neurological diseases. J. Neuroimmunol. 2002, 124:83-92.
87. Town T., Tan J., Flavell R.A., Mullan M. T-cells in Alzheimer's disease. Neruomol. Med. 2005, 7:255-264.
88. 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.
89. von Hundelshausen P., Koenen R.R., Weber C. Platelet-mediated enhancement of leukocyte adhesion. Microcirculation 2009, 16:84-96.
90. Wisniewski H.M., Barcikowska M., Kida E. Phagocytosis of beta/A4 amyloid fibrils of the neuritic neocortical plaques. Acta Neuropathol. 1991, 81:588-590.
91. Wyss-Coray T., Rogers J. Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harbor Perspect. Med. 2012, 2:a006346.
92. Yamada M., Itoh Y., Shintaku M., Kawamura J., Jensson Ó., Thorsteinsson L., Suematsu N., Matsushita M., Otomo E. Immune reactions associated with cerebral amyloid angiopathy. Stroke 1996, 27:1155-1162.
93. Yamanaka M., Ishikawa T., Griep A., Axt D., Kummer M.P., Heneka M.T. PPARγ/RXRα-induced and CD36-mediated microglial amyloid-β phagocytosis results in cognitive improvement in amyloid precursor protein/presenilin 1 mice. J. Neurosci. 2012, 32:17321-17331.
94. Yang Y.M., Shang D.S., Zhao W.D., Fang W.G., Chen Y.H. Microglial TNF-alpha-dependent elevation of MHC class I expression on brain endothelium induced by amyloid-beta promotes T cell transendothelial migration. Neurochem. Res. 2013, 38:2295-2304.
95. Yong V.W., Rivest S. Taking advantage of the systemic immune system to cure brain diseases. Neuron 2009, 64:55-60.
96. Yrlid U., Jenkins C.D., MacPherson G.G. Relationships between distinct blood monocyte subsets and migrating intestinal lymph dendritic cells in vivo under steady-state conditions. J. Immunol. 2006, 176:4155-4162.
97. Zaghi J., Goldenson B., Inayathullah M., Lossinsky A.S., Masoumi A., Avagyan H., Mahanian M., Bernas M., Weinand M., Rosenthal M.J., Espinosa-Jeffrey A., de Vellis J., Teplow D.B., Fiala M. Alzheimer disease macrophages shuttle amyloid-beta from neurons to vessels, contributing to amyloid angiopathy. Acta Neuropathol. 2009, 117:111-124.
98. Zhang W., Huang W., Jing F. Contribution of blood platelets to vascular pathology in Alzheimer's disease. J. Blood Med. 2013, 4:141-147.
99. Ziegler-Heitbrock L. The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 2007, 81:584-592.