APOE genotype alters immunoglobulin subtypes in knock-in mice

Journal of Alzheimer's Disease

Volumn 46, Issue 2, 2015, Pages 365-374

  Zhou, Ye ^a   Zhao, Wenjuan ^b   Al Muhtasib, Nour ^c   Rebeck, G William ^d  

^a UNIVERSITY OF FLORIDA   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c GEORGETOWN UNIVERSITY   (United States)

^d GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apolipoprotein E; brain; immunoglobulin; inflammation; plasma; spleen

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E4; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DETECTION; APOE GENE; ARTICLE; BRAIN; CONTROLLED STUDY; FEMALE; GENE; GENETICALLY ENGINEERED MOUSE STRAIN; GENOTYPE; IMMUNOGLOBULIN BLOOD LEVEL; KNOCK IN MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; ALLELE; ALZHEIMER DISEASE; ANIMAL; BLOOD; C57BL MOUSE; CLASSIFICATION; GENE TARGETING; GENETICS; PLASMA;

ALLELES; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEINS E; BRAIN; FEMALE; GENE KNOCK-IN TECHNIQUES; GENOTYPE; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; PLASMA; SPLEEN;

EID: 84930454840     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-142184     Document Type: Article

References (47)

1. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: High-Avidity binding to beta-Amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci U S A 90, 1977-1981
2. Mahley RW, Rall SC (2000) Apolipoprotein E: Far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1, 507-537
3. Schipper HM (2011) Apolipoprotein E: Implications for AD neurobiology, epidemiology and risk assessment. Neurobiol Aging 32, 778-790
4. Jordan BD, Relkin NR, Ravdin LD, Jacobs AR, Bennett A, Gandy S (1997) Apolipoprotein E epsilon4 associated with chronic traumatic brain injury in boxing. JAMA 278, 136-140
5. Corder EH, Saunders AM, Risch NJ, Strittmatter WJ, Schmechel DE, Gaskell PC Jr, Rimmler JB, Locke PA, Conneally PM, Schmader KE (1994) Protective effect of apolipoproteinEtype 2 allele for late onset Alzheimer disease. Nat Genet 7, 180-184
6. Verghese PB, Castellano JM, Garai K, Wang Y, Jiang H, Shah A, Bu G, Frieden C, Holtzman DM (2013) ApoE influences amyloid-(A-) clearance despite minimal apoE/A-Association in physiological conditions. Proc Natl Acad Sci U S A 110, E1807-E1816
7. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63, 287-303
8. Lee CYD, Landreth GE (2010) The role of microglia in amyloid clearance from the AD brain. J Neural Transm 117, 949-960
9. Zhao W, Zhang J, Davis EG, Rebeck GW (2014) Aging reduces glial uptake and promotes extracellular accumulation of A-from a lentiviral vector. Front Aging Neurosci 6, 210
10. Liu C-C, Liu C-C, Kanekiyo T, Xu H, Bu G (2013) Apolipoprotein E and Alzheimer disease: Risk, mechanisms and therapy. Nat Rev Neurol 9, 106-118
11. Van Ree JH, van den Broek WJ, Dahlmans VE, Groot PH, Vidgeon-Hart M, Frants RR, Wieringa B, Havekes LM, Hofker MH (1994) Diet-induced hypercholesterolemia and atherosclerosis in heterozygous apolipoprotein E-deficient mice. Atherosclerosis 111, 25-37
12. Sullivan PM, Mezdour H, Aratani Y, Knouff C, Najib J, Reddick RL, Quarfordt SH, Maeda N (1997) Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 272, 17972-17980
13. Vitek MP, Brown CM, Colton CA (2009) APOE genotypespecific differences in the innate immune response. Neurobiol Aging 30, 1350-1360
14. Lynch JR, Tang W, Wang H, Vitek MP, Bennett ER, Sullivan PM, Warner DS, Laskowitz DT (2003) APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. J Biol Chem 278, 48529-48533
15. Zhu Y, Nwabuisi-Heath E, Dumanis SB, Tai LM, Yu C, Rebeck GW, LaDu MJ (2012) APOE genotype alters glial activation and loss of synaptic markers in mice. Glia 60, 559-569
16. Stavnezer J (1996) Immunoglobulin class switching. Curr Opin Immunol 8, 199-205
17. Zhao W, Dumanis SB, Tamboli IY, Rodriguez GA, LaDu MJ, Moussa CEH, Rebeck GW (2014) Human APOE genotype affects intraneuronalA-1-42 accumulation in a lentiviral gene transfer model. Hum Mol Genet 23, 1365-1375
18. Rodriguez GA, TaiLM, LaDuMJ, RebeckGW(2014)Human APOE4 increases microglia reactivity at A-plaques in a mouse model ofA-deposition. J Neuroinflammation 11, 111
19. Kawano Y, Noma T, Yata J (1994) Regulation of human IgG subclass production by cytokines. IFN-gamma and IL-6 act antagonistically in the induction of human IgG1 but additively in the induction of IgG2. J Immunol 153, 4948-4958
20. Reardon CA, Blachowicz L, White T, Cabana V, Wang Y, Lukens J, Bluestone J, Getz GS (2001) Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 21, 1011-1016
21. Barger SW, Harmon AD (1997) Microglial activation by Alzheimer amyloid precursor protein and modulation by apolipoprotein E. Nature 388, 878-881
22. Youmans KL, Tai LM, Nwabuisi-Heath E, Jungbauer L, Kanekiyo T, Gan M, Kim J, EimerWA, Estus S, RebeckGW, Weeber EJ, Bu G, Yu C, Ladu MJ (2012) APOE4-specific changes inA-Accumulation in a newtransgenic mouse model of Alzheimer disease. J Biol Chem 287, 41774-41786
23. Nelson PT, Pious NM, Jicha GA, Wilcock DM, Fardo DW, Estus S, Rebeck GW (2013) APOE-2 and APOE-4 correlate with increased amyloid accumulation in cerebral vasculature. J Neuropathol Exp Neurol 72, 708-715
24. Kelly ME, Clay MA, Mistry MJ, Hsieh-Li HM, Harmony JA (1994) Apolipoprotein E inhibition of proliferation of mitogen-Activated T lymphocytes: Production of interleukin 2 with reduced biological activity. Cell Immunol 159, 124-139
25. Pocivavsek A, Burns MP, Rebeck GW (2009) Low-density lipoprotein receptors regulate microglial inflammation through c-Jun N-terminal kinase. Glia 57, 444-453
26. Campos-Rodríguez R, Godínez-Victoria M, Abarca-Rojano E, Pacheco-Yépez J, Reyna-Garfias H, Barbosa-Cabrera RE, Drago-Serrano ME (2013) Stress modulates intestinal secretory immunoglobulin A. Front Integr Neurosci 7, 86
27. Correale J, Villa A (2004) The neuroprotective role of inflammation in nervous system injuries. J Neurol 251, 1304-1316
28. Weinstein JS, Hernandez SG, Craft J (2012) T cells that promote B-Cell maturation in systemic autoimmunity. Immunol Rev 247, 160-171
29. Tai LM, Mehra S, Shete V, Estus S, Rebeck GW, Bu G, LaDu MJ (2014) Soluble apoE/A-complex: Mechanism and therapeutic target for APOE4-induced AD risk. Mol Neurodegener 9, 2
30. Kalinin S, Richardson JC, Feinstein DL (2009) A PPARdelta agonist reduces amyloid burden and brain inflammation in a transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 6, 431-437
31. Guo L, LaDu MJ, Van Eldik LJ (2004) A dual role for apolipoprotein E in neuroinflammation: Anti-And proinflammatory activity. J Mol Neurosci 23, 205-212
32. Pocivavsek A, Mikhailenko I, Strickland DK, Rebeck GW (2009) Microglial low-density lipoprotein receptor-related protein 1 modulates c-Jun N-terminal kinase activation. J Neuroimmunol 214, 25-32
33. Pocivavsek A, Rebeck GW (2009) Inhibition of c-Jun Nterminal kinase increases apoE expression in vitro and in vivo. Biochem Biophys Res Commun 387, 516-520
34. May P, Bock HH, Nofer J-R (2013) Low density receptorrelated protein 1 (LRP1) promotes anti-inflammatory phenotype in murine macrophages. Cell Tissue Res 354, 887-889
35. Lei B, Mace B, Bellows ST, Sullivan PM, Vitek MP, Laskowitz DT, James ML (2012) Interaction between sex and apolipoprotein e genetic background in a murine model of intracerebral hemorrhage. Transl Stroke Res 3, 94-101
36. Laskowitz DT, Horsburgh K, Roses AD (1998) Apolipoprotein E and the CNS response to injury. J Cereb Blood Flow Metab 18, 465-471
37. Bateman RJ, Xiong C, Benzinger TLS, Fagan AM, Goate A, Fox NC, Marcus DS, Cairns NJ, Xie X, Blazey TM, Holtzman DM, Santacruz A, BucklesV, OliverA, Moulder K, Aisen PS, Ghetti B, Klunk WE, McDade E, Martins RN, Masters CL, Mayeux R, Ringman JM, Rossor MN, Schofield PR, Sperling RA, Salloway S, Morris JC (2012) Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N Engl J Med 367, 795-804
38. Fillit H, Hess G, Hill J, Bonnet P, Toso C (2009) IV immunoglobulin is associated with a reduced risk of Alzheimer disease and related disorders. Neurology 73, 180-185
39. Schwab I, Nimmerjahn F (2013) Intravenous immunoglobulin therapy: How does IgG modulate the immune system?. Nat Rev Immunol 13, 176-189
40. Britschgi M, Olin CE, Johns HT, Takeda-Uchimura Y, LeMieux MC, Rufibach K, Rajadas J, Zhang H, Tomooka B, Robinson WH, Clark CM, Fagan AM, Galasko DR, Holtzman DM, Jutel M, Kaye JA, Lemere CA, Leszek J, Li G, Peskind ER, Quinn JF, Yesavage JA, Ghiso JA, Wyss-Coray T (2009) Neuroprotective natural antibodies to assemblies of amyloidogenic peptides decrease with normal aging and advancing Alzheimer's disease. Proc Natl Acad Sci U S A 106, 12145-12150
41. Nimmerjahn F, Ravetch JV (2008) Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol 26, 513-533
42. Sudduth TL, Greenstein A, Wilcock DM (2013) Intracranial injection of gammagard, a human IVIg, modulates the inflammatory response of the brain and lowers A-in APP/PS1 mice along a different time course than anti-A-Antibodies. J Neurosci 33, 9684-9692
43. Relkin N (2014) Clinical trials of intravenous immunoglobulin for Alzheimer's disease. J Clin Immunol 34(Suppl 1), S74-S79
44. Salloway S, Sperling R, Fox NC, Blennow K, Klunk W, Raskind M, Sabbagh M, Honig LS, Porsteinsson AP, Ferris S, Reichert M, Ketter N, Nejadnik B, Guenzler V, Miloslavsky M, Wang D, LuY, Lull J, Tudor IC, Liu E, Grundman M, Yuen E, Black R, Brashear HR (2014) Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N Engl J Med 370, 322-333
45. Sakai K, Boche D, Carare R, Johnston D, Holmes C, Love S, Nicoll JAR (2014) A-immunotherapy for Alzheimer's disease: Effects on apoE and cerebral vasculopathy. Acta Neuropathol (Berl) 128, 777-789
46. Chen Y, Durakoglugil MS, Xian X, Herz J (2010) ApoE4 reduces glutamate receptor function and synaptic plasticity by selectively impairing ApoE receptor recycling. Proc Natl Acad Sci U S A 107, 12011-12016
47. Fuller JP, Stavenhagen JB, Teeling JL (2014) Newroles for Fc receptors in neurodegeneration-the impact on immunotherapy for Alzheimer's disease. Front Neurosci 8, 235