CC chemokine receptor 2 deficiency aggravates cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease

Journal of Neuroscience

Volumn 31, Issue 16, 2011, Pages 6208-6220

  Naert, Gaelle ^a   Rivest, Serge ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1;

AGING; ALZHEIMER DISEASE; AMNESIA; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN CORTEX; COGNITIVE DEFECT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE COURSE; DISEASE EXACERBATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENETIC ASSOCIATION; MALE; MENTAL DETERIORATION; MICROGLIA; MOLECULAR PATHOLOGY; MOUSE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEFICIENCY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LINEAR MODELS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, TRANSGENIC; MICROGLIA; PLAQUE, AMYLOID; PRESENILIN-1; RECEPTORS, CCR2; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79955775349     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0299-11.2011     Document Type: Article

References (82)

1. Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C, Saederup N, Leemput J, Bigot K, Campisi L, Abitbol M, Molina T, Charo I, Hume DA, Cumano A, Lauvau G, Geissmann F (2009) CX3CR1+ CD115 + CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 206:595-606.
2. Babcock AA, Kuziel WA, Rivest S, Owens T (2003) Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neu-rosci 23:7922-7930.
3. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneu-ronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45:675-688.
4. Boissonneault V, Filali M, Lessard M, Relton J, Wong G, Rivest S (2009) Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 132:1078-1092.
5. Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME (2008) Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 28:4283-4292.
6. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19:939-945.
7. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T (2003) Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40:1133-1145.
8. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924.
9. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354:610-621.
10. Cheng IH, Scearce-Levie K, Legleiter J, Palop JJ, Gerstein H, Bien-Ly N, Puolivali J, Lesne S, Ashe KH, Muchowski PJ, Mucke L (2007) Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem 282:23818-23828.
11. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84.
12. Cruz JC, Kim D, Moy LY, Dobbin MM, Sun X, Bronson RT, Tsai LH (2006) p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloidβ- in vivo. J Neurosci 26:10536-10541.
13. Cushing SD, Berliner JA, Valente AJ, Territo MC, Navab M, Parhami F, Gerrity R, Schwartz CJ, Fogelman AM (1990) Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci U S A 87:5134-5138.
14. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, et al. (2003) RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9:907-913.
15. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, Hu HW, Spijkers P, Guo H, Song X, Lenting PJ, Van Nostrand WE, Zlokovic BV (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43:333-344.
16. DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM, Holtzman DM (2001) Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 98:8850-8855.
17. Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoat-tractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313-326.
18. D'Mello C, Le T, Swain MG (2009) Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J Neurosci 29:2089-2102.
19. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, Luster AD (2003) CD36 mediates the innate host response to beta-amyloid. J Exp Med 197:1657-1666.
20. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13:432-438.
21. high monocytes from the bone marrow, but is dispensable for bladder infiltration in bacterial urinary tract infection. J Immunol 181:5579-5586.
22. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, Haass C, LaFerla FM, Kretzschmar H, Herms J (2010) Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 13:411-413.
23. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82.
24. Glabinski AR, Balasingam V, Tani M, Kunkel SL, Strieter RM, Yong VW, Ransohoff RM (1996) Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J Immunol 156:4363-4368.
25. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156:15-20.
26. Gouras GK, Almeida CG, Takahashi RH (2005) Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol Aging 26:1235-1244.
27. Grammas P, Ovase R (2001) Inflammatory factors are elevated in brain mi-crovessels in Alzheimer's disease. Neurobiol Aging 22:837-842.
28. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8:101-112.
29. Harrison JK, Jiang Y,Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Feng L (1998) Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 95:10896-10901.
30. Holtzman DM, Bales KR, Paul SM, DeMattos RB (2002) Abeta immunization and anti-Abeta antibodies: potential therapies for the prevention and treatment of Alzheimer's disease. Adv Drug Deliv Rev 54:1603-1613.
31. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
32. Ishizuka K, Kimura T, Igata-yi R, Katsuragi S, Takamatsu J, Miyakawa T (1997) Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease. Psychiatry Clin Neurosci 51:135-138.
33. Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD (2000) Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 192:1075-1080.
34. Jia T, Serbina NV, Brandl K, Zhong MX, Leiner IM, Charo IF, Pamer EG (2008) Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol 180:6846-6853.
35. Kawarabayashi T, Shoji M, Younkin LH, Wen-Lang L, Dickson DW, Murakami T, Matsubara E, Abe K, Ashe KH, Younkin SG (2004) Di-meric amyloidβ- protein rapidly accumulates in lipid rafts followed by apolipoprotein E and phosphorylated tau accumulation in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 24:3801-3809.
36. Knobloch M, Konietzko U, Krebs DC, Nitsch RM (2007) Intracellular Abeta and cognitive deficits precede beta-amyloid deposition in transgenic arcAbeta mice. Neurobiol Aging 28:1297-1306.
37. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8:499-509.
38. Laflamme N, Rivest S (2001) Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J 15:155-163.
39. Laflamme N, Lacroix S, Rivest S (1999) An essential role of interleukin-1β- in mediating NF-kB activity and COX-2 transcription in cells of the blood-brain barrier in response to a systemic and localized inflammation but not during endotoxemia. J Neurosci 19:10923-10930.
40. Lemere CA, Spooner ET, LaFrancois J, Malester B, Mori C, Leverone JF, Matsuoka Y, Taylor JW, DeMattos RB, Holtzman DM, Clements JD, Selkoe DJ, Duff KE (2003) Evidence for peripheral clearance of cerebral Abeta protein following chronic, active Abeta immunization in PSAPP mice. Neurobiol Dis 14:10-18.
41. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
42. Lesne S, Kotilinek L, Ashe KH (2008) Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience 151:745-749.
43. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA (2006) Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24:99-146.
44. 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.
45. Luster AD (1998) Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 338:436-445.
46. Mack M, Cihak J, Simonis C, Luckow B, Proudfoot AE, Plachy J, Brühl H, Frink M, Anders HJ, Vielhauer V, Pfirstinger J, Stangassinger M, Schlon-dorff D (2001) Expression and characterization of the chemokine receptors CCR2 and CCR5 in mice. J Immunol 166:4697-4704.
47. Malm TM, Koistinaho M, Parepalo M, Vatanen T, Ooka A, Karlsson S, Kois-tinaho J (2005) 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 18:134-142.
48. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Lan-dreth GE (2009) Microglia mediate the clearance of soluble Aβ- through fluid phase macropinocytosis. J Neurosci 29:4252-4262.
49. Matsunaga W, Shirokawa T, Isobe K (2003) Specific uptake of Abeta1-40 in rat brain occurs in astrocyte, but not in microglia. Neurosci Lett 342:129-131.
50. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46: 860-866.
51. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
52. Meilandt WJ, Cisse M, Ho K, Wu T, Esposito LA, Scearce-Levie K, Cheng IH, Yu GQ, Mucke L (2009) Neprilysin overexpression inhibits plaque formation but fails to reduce pathogenic Aβ- oligomers and associated cognitive deficits in human amyloid precursor protein transgenic mice. J Neurosci 29:1977-1986.
53. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969.
54. Mousseau DD, Chapelsky S, De Crescenzo G, Kirkitadze MD, Magoon J, Inoue S, Teplow DB, O'Connor-McCourt MD (2003) A direct interaction between transforming growth factor (TGF)-betas and amyloid-beta protein affects fibrillogenesis in a TGF-beta receptor-independent manner. J Biol Chem 278:38715-38722.
55. Nadeau S, Rivest S (2000) Role of microglial-derived tumor necrosis factor in mediating CD14 transcription and nuclear factor-KB activity in the brain during endotoxemia. J Neurosci 20:3456-3468.
56. Naert G, Laflamme N, Rivest S (2009) Toll-like receptor 2-independent and MyD88-dependent gene expression in the mouse brain. J Innate Immun 1:480-493.
57. Nielsen HM, Veerhuis R, Holmqvist B, Janciauskiene S (2009) Binding and uptake of A beta1-42 by primary human astrocytes in vitro. Glia 57:978-988.
58. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneu-ronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 26:10129-10140.
59. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
60. Perry VH, Gordon S (1988) Macrophages and microglia in the nervous system. Trends Neurosci 11:273-277.
61. Peters I, Igbavboa U, Schütt T, Haidari S, Hartig U, Rosello X, Bottner S, Copanaki E, Deller T, Kogel D, Wood WG, Müller WE, Eckert GP (2009) The interaction of beta-amyloid protein with cellular membranes stimulates its own production. Biochim Biophys Acta 1788:964-972.
62. Richard KL, Filali M, Prefontaine P, Rivest S (2008) Toll-like receptor 2 acts as anatural innate immune receptor to clear amyloidβ- 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J Neurosci 28:5784-5793.
63. Rollins BJ, Yoshimura T, Leonard EJ, Pober JS (1990) Cytokine-activated human endothelial cells synthesize and secrete a monocyte chemoattrac-tant, MCP-1/JE. Am J Pathol 136:1229-1233.
64. Rota E, Bellone G, Rocca P, Bergamasco B, Emanuelli G, Ferrero P (2006) Increased intrathecal TGF-β-1, but not IL-12, IFN-y and IL-10 levels in Alzheimer's disease patients. Neurol Sci 27:33-39.
65. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
66. Selkoe DJ (2008) Biochemistry and molecular biology of amyloid beta-protein and the mechanism of Alzheimer's disease. Handb Clin Neurol 89:245-260.
67. Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7:311-317.
68. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, Ghiso J, Zlokovic BV (2000) Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106:1489-1499.
69. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502.
70. Smits HA, Rijsmus A, van Loon JH, Wat JW, Verhoef J, Boven LA, Nottet HS (2002) Amyloid-beta-induced chemokine production in primary human macrophages and astrocytes. J Neuroimmunol 127:160-168.
71. Stalder AK, Ermini F, Bondolfi L, Krenger W, Burbach GJ, Deller T, Cooma-raswamy J, Staufenbiel M, Landmann R, Jucker M (2005) Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J Neurosci 25:11125-11132.
72. Steinerman JR, Irizarry M, Scarmeas N, Raju S, Brandt J, Albert M, Blacker D, Hyman B, Stern Y (2008) Distinct pools of beta-amyloid in Alzheimer disease-affected brain: a clinicopathologic study. Arch Neurol 65:906-912.
73. Tampellini D, Rahman N, Gallo EF, Huang Z, Dumont M, Capetillo-Zarate E, Ma T, Zheng R, Lu B, Nanus DM, Lin MT, Gouras GK (2009) Synaptic activity reduces intraneuronal Aβ-, promotes APP transport to synapses, and protects against Aβ-related synaptic alterations. J Neurosci 29:9704-9713.
74. Town T, Laouar Y, Pittenger C, Mori T, Szekely CA, Tan J, Duman RS, Flavell RA (2008) Blocking TGF-beta-Smad2β- innate immune signaling mitigates Alzheimer-like pathology. Nat Med 14:681-687.
75. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF (2007) Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 117:902-909.
76. van der Wal EA, Gómez-Pinilla F, Cotman CW (1993) Transforming growth factor-beta 1 is in plaques in Alzheimer and Down pathologies. Neuroreport 4:69-72.
77. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, Kal-chenko V, Geissmann F, Jung S (2007) Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 204:171-180.
78. Varol C, Yona S, Jung S (2009) Origins and tissue-context-dependent fates of blood monocytes. Immunol Cell Biol 87:30-38.
79. Wirths O, Multhaup G, Bayer TA (2004) A modified beta-amyloid hypoth- esis: intraneuronal accumulation of the beta-amyloid peptide-the first step of a fatal cascade. J Neurochem 91:513-520.
80. Wyss-Coray T, Masliah E, Mallory M, McConlogue L, Johnson-Wood K, Lin C, Mucke L (1997) Amyloidogenic role of cytokine TGF-beta1 in trans-genic mice and in Alzheimer's disease. Nature 389:603-606.
81. Wyss-Coray T, Lin C, Sanan DA, Mucke L, Masliah E (2000) Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol 156:139-150.
82. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L (2001) TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 7:612-618.