Transplanted astrocytes internalize deposited β-amyloid peptides in a transgenic mouse model of Alzheimer's disease

GLIA

Volumn 56, Issue 2, 2008, Pages 154-163

  Pihlaja, Rea ^a   Koistinaho, Jari ^a,b   Malm, Tarja ^a   Sikkilä, Herkko ^c   Vainio, Seppo ^c   Koistinaho, Milla ^a,d  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d Medeia Therapeutics Ltd   (Finland)

Author keywords

Animal model; Enhanced green fluorescence protein; Glia; Phagocytosis; Transplantation

Indexed keywords

AMYLOID BETA PROTEIN; GREEN FLUORESCENT PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN; CELL CULTURE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL MOVEMENT; CELL TRANSPLANTATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IMAGING, THREE-DIMENSIONAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MUTATION; PRESENILIN-1;

EID: 37349114621     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20599     Document Type: Article

References (41)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T. 2000. Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
2. Arnhold S, Kreppel F, Kandirali S, Lenartz D, Klintz FJ, Sturm V, Kochanek S, Anderssen C, Addicks K. 2002. Intracerebral transplantation and successful integration of astrocytes following genetic modification with a high-capacity adenoviral vector. Cell Transplant 11:663-670.
3. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. 1998. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats - Similarities to astrocyte grafts. Proc Natl Acad Sci USA 95:3908-3913.
4. Bacskai BJ, Kajdasz ST, McLellan ME, Games D, Seubert P, Schenk D, Hyman BT 2002. Non-Fc-mediated mechanisms are involved in clearance of amyloid-β in vivo by immunotherapy. J Neurosci 22: 7873-7878.
5. Bakhiet M, Mousa A, Seiger A, Andersson J. 2002. Constitutive and inflammatory induction of α and β chemokines in human first trimester forebrain astrocytes and neurons. Mol Immunol 38:921-929.
6. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T. 2000. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
7. 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.
8. Chao CC, Hu S, Ehrlich L, Peterson PK. 1995. Interleukin-1 and tumor necrosis factor-α synergistically mediate neurotoxicity: Involvement of nitric oxide and of N-methyl-D-aspartate receptors. Brain Behav Immun 9:355-365.
9. DeWitt DA, Perry G, Cohen M, Doller C, Silver J. 1998. Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exp Neurol 149:329-340.
10. German DC, Eisch AJ. 2004. Mouse models of Alzheimer's disease: Insight into treatment. Rev Neurosci 15:353-369.
11. Gitter BD, Cox LM, Rydel RE, May PC. 1995. Amyloid β peptide potentiates cytokine secretion by interleukin-1 β-activated human astrocytoma cells. Proc Natl Acad Sci USA 92:10738-10741.
12. Gotz J, Streffer JR, David D, Schild A, Hoerndli F, Pennanen L, Kurosinski P, Chen F. 2004. Transgenic animal models of Alzheimer's disease and related disorders: Histopathology, behavior and therapy. Mol Psychiatry 9:664-683.
13. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzie JE, Graham DI, Roberts GW, Mrak RE. 1998. Glial-neuronal interactions in Alzheimer's disease: The potential role of a 'cytokine cycle' in disease progression. Brain Pathol 8:65-72.
14. Haga S, Akai K, Ishii T 1989. Demonstration of microglial cells in and around senile (neuritic) plaques in the Alzheimer brain. An immunohistochemical study using a novel monoclonal antibody. Acta Neuropathol (Berl) 77:569-575.
15. Hardy J, Duff K, Hardy KG, Perez-Tur J, Hutton M. 1998. Genetic dissection of Alzheimer's disease and related dementias: Amyloid and its relationship to tau. Nat Neurosci 1:355-358.
16. Higgins LS, Rodems JM, Catalano R, Quon D, Cordell B. 1995. Early Alzheimer disease-like histopathology increases in frequency with age in mice transgenic for β-APP751. Proc Natl Acad Sci USA 92:4402-4406.
17. Hu J, Akama KT, Krafft GA, Chromy BA, Van Eldik LJ. 1998. Amyloid-β peptide activates cultured astrocytes: Morphological alterations, cytokine induction and nitric oxide release. Brain Res 785:195-206.
18. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D. 1989. Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J Neuroimmunol 24:173-182.
19. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR. 2004. Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: Evidence for augmentation of a 42-specific γ secretase. Hum Mol Genet 13:159-170.
20. Kalback W, Watson MD, Kokjohn TA, Kuo YM, Weiss N, Luehrs DC, Lopez J, Brune D, Sisodia SS, Staufenbiel M, Emmerling M, Roher AE. 2002. APP transgenic mice Tg2576 accumulate Aβ peptides that are distinct from the chemically modified and insoluble peptides deposited in Alzheimer's disease senile plaques. Biochemistry 41:922-928.
21. Koistinaho M, Koistinaho J. 2002. Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40:175-183.
22. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM. 2004. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-β peptides. Nat Med 10:719-726.
23. Kuo YM, Kokjohn TA, Beach TG, Sue LI, Brune D, Lopez JC, Kalback WM, Abramowski D, Sturchler-Pierrat C, Staufenbiel M, Roher AE. 2001. Comparative analysis of amyloid-β chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J Biol Chem 276:12991-12998.
24. Matsunaga W, Shirokawa T, Isobe K. 2003. Specific uptake of Aβ1-40 in rat brain occurs in astrocyte, but not in microglia. Neurosci Lett 342:129-131.
25. Mattson MP. 2004. Pathways towards and away from Alzheimer's disease. Nature 430:631-639.
26. Nagele RG, D'Andrea MR, Lee H, Venkataraman V, Wang HY. 2003. Astrocytes accumulate Aβ 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 971:197-209.
27. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 1997. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 407:313-319.
28. Pencalet P, Serguera C, Corti O, Privat A, Mallet J, Gimenez y Ribotta M. 2006. Integration of genetically modified adult astrocytes into the lesioned rat spinal cord. J Neurosci Res 83:61-67.
29. Price DL, Tanzi RE, Borchelt DR, Sisodia SS. 1998. Alzheimer's disease: Genetic studies and transgenic models. Annu Rev Genet 32:461-493.
30. Roher AE, Palmer KC, Yurewicz EC, Ball MJ, Greenberg BD. 1993. Morphological and biochemical analyses of amyloid plaque core proteins purified from Alzheimer disease brain tissue. J Neurochem 61:1916-1926.
31. Rojas-Fernandez CH, Chen M, Fernandez HL. 2002. Implications of amyloid precursor protein and subsequent β-amyloid production to the pharmacotherapy of Alzheimer's disease. Pharmacotherapy 22:1547-1556.
32. Selkirk SM, Greenberg SJ, Plunkett RJ, Barone TA, Lis A, Spence PO. 2002. Syngeneic central nervous system transplantation of genetically transduced mature, adult astrocytes. Gene Ther 9:432-443.
33. Selkoe DJ. 2001. Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 81:741-766.
34. Selkoe DJ, Abraham CR, Podlisny MB, Duffy LK. 1986. Isolation of low-molecular-weight proteins from amyloid plaque fibers in Alzheimer's disease. J Neurochem 46:1820-1834.
35. Sommer B. 2002. Alzheimer's disease and the amyloid cascade hypothesis: Ten years on. Curr Opin Pharmacol 2:87-92.
36. Suh YH, Checler F. 2002. Amyloid precursor protein, presenilins, and a-synuclein: Molecular pathogenesis and pharmacological applications in Alzheimer's disease. Pharmacol Rev 54:469-525.
37. Wallace MN, Geddes JG, Farquhar DA, Masson MR. 1997. Nitric oxide synthase in reactive astrocytes adjacent to β-amyloid plaques. Exp Neurol 144:266-272.
38. Wegiel J, Wang KC, Tarnawski M, Lach B. 2000. Microglia cells are the driving force in fibrillar plaque formation, whereas astrocytes are a leading factor in plague degradation. Acta Neuropathol (Berl) 100:356-364.
39. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L. 2001. TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice. Nat Med 7:612-618.
40. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J. 2003. Adult mouse astrocytes degrade amyloid-β in vitro and in situ. Nat Med 9:453-457.
41. Yin K-J, Cirrito JR, Yan Ping, Hu X, Xiao Q, Pan X, Bateman R, Song H, Hsu F-F, Turk J, Xu J, Hsu CY, Mills JC, Holtzman DM, Lee J-M. 2006. Matrix metalloproteinases expressed by astrocytes mediate extracellular amyloid-β peptide catabolism. J Neurosci 26:10939-10948.