Intracerebral transplantation of bone marrow-derived mesenchymal stem cells reduces amyloid-beta deposition and rescues memory deficits in Alzheimer's disease mice by modulation of immune responses

Stem Cells

Volumn 28, Issue 2, 2010, Pages 329-343

  Lee, Jong Kil ^a   Jin, Hee Kyung ^a   Endo, Shogo ^b   Schuchman, Edward H ^c   Carter, Janet E ^d   Bae, Jae Sung ^a  

^a Kyungpook National University   (South Korea)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Alternatively activated microglia; Alzheimer's disease model; Amyloid ; transplantation; Bone marrow derived mesenchymal stem cell

Indexed keywords

AMYLOID BETA PROTEIN; PRESENILIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; BRAIN REGION; COGNITION; CONTROLLED STUDY; IMMUNE RESPONSE; INFLAMMATION; LEARNING; MESENCHYMAL STEM CELL; MICROGLIA; MOUSE; NEUROFIBRILLARY TANGLE; NONHUMAN; PHENOTYPE; PROTEIN PHOSPHORYLATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; MAZE LEARNING; MEMORY DISORDERS; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, TRANSGENIC; PRESENILIN-1;

MUS; MUS MUSCULUS;

EID: 77149146814     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.277     Document Type: Article

References (59)

1. Selkoe DJ. Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 2001;81:741-766.
2. HuttonM,McGowan E. Clearing tau pathology with abeta immunotherapy - reversible and irreversible stages revealed. Neuron 2004;43:293-294.
3. Busciglio J, Lorenzo A, Yeh J et al. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 1995;14: 879-888.
4. Mattson MP. Pathways towards and away from Alzheimer's disease. Nature 2004;430:631-639.
5. Bantubungi K, Blum D, Cuvelier L et al. Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease. Mol Cell Neurosci 2008;37:454-470.
6. Cho YH, Kim HS, Lee KH et al. The behavioral effect of human mesenchymal stem cell transplantation in cold brain injured rats. Acta Neurochir Suppl 2006;99:125-132.
7. Bae JS, Furuya S, Shinoda Y et al. Neurodegeneration augments the ability of bone marrow-derived mesenchymal stem cells to fuse with Purkinje neurons in Niemann-Pick type C mice. Hum Gene Ther 2005;16:1006-1011.
8. Lee JK, Jin HK, Bae JS. Bone marrow-derived mesenchymal stem cells reduce brain amyloid-beta deposition and accelerate the activation of microglia in an acutely induced Alzheimer's disease mouse model. Neurosci Lett 2009;450:136-141.
9. Wegiel J, Wang KC, Imaki H et al. The role of microglial cells and astrocytes in fibrillar plaque evolution in transgenic APP(SW) mice. Neurobiol Aging 2001;22:49-61.
10. Malm TM, Koistinaho M, Parepalo M et al. Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzehimer mice. Neurobiol Dis 2005;18:134-142.
11. Simard AR, Soulet D, Gowing G et al. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006;49:489-502.
12. Coraci IS, Husemann J, Berman JW et al. 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.
13. El Khoury JB, Moore KJ, Means TK et al. CD36 mediates the innate host response to beta amyloid. J Exp Med 2003;197:1657-1666.
14. Meda L, Cassatella MA, Szendrei GI et al. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 1995;374: 647-650.
15. Rogers J, Strohmeyer R, Kovelowski CJ et al. Microglia and inflammatory mechanisms in the clearance of amyloid beta peptide. Glia 2002;40:260-269.
16. Chung H, Brazil MI, Soe Ttet al. Uptake, degradation, and release of fibrillar and soluble forms of Alzheimer's amyloid beta peptide by microglial cells. J Biol Chem 1999;274:32301-32308.
17. Ohtaki H, Ylostalo JH, Foraker JE et al. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune response. Proc Natl Acad Sci U S A 2008;105:14638-14643.
18. Howlett DR, Richardson JC, Austin A et al. Cognitive correlates of Abeta deposition in male and female mice bearing amyloid precursor protein and presenilin-1 mutant transgene. Brain Res 2004;1017: 130-136.
19. Näslund J, Haroutunian V, Mohs R et al. Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 2000;283:1571-1577.
20. Koistinaho M, Ort M, Cimadevilla JM et al. Specific spatial learning deficits become severe with age in beta-amyloid precursor protein transgenic mice that harbor diffuse beta-amyloid deposits but do not form plaques. Proc Natl Acad Sci U S A 2001;98:14675-14680.
21. Leissring MA, Farris W, Chang AY et al. Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 2003;40:1087-1093.
22. Yan P, Hu X, Song H et al. Matrix metalloproteinase-9 degrades amyloid-beta fibrils in vitro and compact plaques in situ. J Biol Chem 2006;281:24566-24574.
23. Yan SD, Chen X, Fu J et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996;382:685-691.
24. El Khoury J, Hickman SE, Thomas CA et al. Microglia, scavenger receptor, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 1998;19:S81-S84.
25. Hickman SE, Allison EK, El Khoury J. Microglial dysfunction and defective beta-amyloid clearance pathway in aging Alzheimer's disease mice. J Neurosci 2008;28:8354-8360.
26. Heneka MT, O'Banion MK. Inflammatory processes in Alzheimer's disease. J Neuroimmunol 2007;184:69-91.
27. Janelsins MC, Mastrangelo MA, Oddo S et al. Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice. J Neuroinflammation 2005;2:23.
28. Gordon S. Alternative activation of macrophage. Nat Rev Immunol 2003;3:23-35.
29. Edwards JP, Zhang X, Frauwirth KA et al. Biochemical and functional characterization of three activated macrophage population. J Leukoc Biol 2006;80:1298-1307.
30. Roberson ED, Scearce-Levie K, Palop JJ et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007;316:750-754.
31. Howlett DR, Bowler K, Soden PE et al. Aβ deposition and related pathology in an APP x PS1 transgenic mouse model of Alzheimer's disease. Histol Histopathol 2008;23:67-76.
32. Blurton-Jones M, LaFerla FM. Pathway by which Abeta facilitates tau pathology. Curr Alzheimer Res 2006;3:437-448.
33. El Khoury J, Toft M, Hickman SE et al. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer's-like disease. Nat Med 2007;13:432-438.
34. Iwata N, Tsubuki S, Takaki Y et al. Metabolic regulation of brain Abeta by neprilysin. Science 2001;292:1550-1552.
35. Richard KL, Filali M, Préfontaine P et al. 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 of Alzheimer's disease. J Neurosci 2008;28:5784-5793.
36. Farris W, Mansourian S, Chang Yet al. Insukin-degrading enzyme regulates the levels of insulin, amyloid beta protein, the β-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA. 2003;100:4162-4167.
37. Yasojima K, Akiyama H, McGeer EG et al. Reduced neprilysin in high plaque areas of Alzheimer brain: A possible relationship to deficient degradation of beta-amyloid peptides. Neurosci Lett 2001;297: 97-100.
38. Boissonneault V, Filali M, Lessard M et al. Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 2009;132: 1072-1092.
39. Pérez A, Morelli L, Cresto JC et al. Degradation of soluble amyloid beta-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brain. Neurochem Res 2000;25:247-255.
40. Zhao J, Xiang Z, Haroutunian V et al. Insulin degrading enzyme activity selectivrly decreases in the hippocampal formation of cases at high risk to develop Alzheimer's disease. Neurobiol Aging 2007;28: 824-830.
41. Walker DJ, Link J, Lue JF et al. Gene expression changes by amyloid beta peptide-stimulated human postmortem brain microglia identify activation of multiple inflammatory processes. J Leukoc Biol 2006;79: 596-610.
42. Rosenberg PB. Clinical aspects of inflammation in Alzheimer's disease. Int Rev Psychiatry 2005;17:503-514.
43. Ponomarev ED, Maresz K, Tan Y et al. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci 2007;27: 10714-10721.
44. Iribarren P, Chen K, Hu J et al. IL-4 inhibits the expression of mouse formyl peptide receptor 2, a receptor for amyloid beta 1-42, in TNF-alpha-activated microglia. J Immunol 2005;175:6100-6106.
45. Falcone M, Rajan AJ, Bloom BR et al. A critical role for IL-4 in regulating disease severity in experimental allergic encephalomyelitis as demonstrated in IL-4-deficient C57BL/6 mice and BALB/c mice. J Immunol 1998;160:4822-4830.
46. Koenigsknecht-Talboo J, Landreth GE. Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 2005;25:8240-8249.
47. Stein M, Keshav S, Harris N et al. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J Exp Med 1992;176:287-292.
48. Butovsky O, Talpalar AE, Ben-Yaakov K et al. Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHCII expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol Cell Neurosci 2005;29:381-393.
49. Zhao W, Xie W, Xiao Q et al. Protective effectives of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J Neurochem 2006;99:1176-1187.
50. Butovsky O, Koronyo-Hamaoui M, Kunis G et al. Glatiramer acetate fights against Alzheimer's disease by inducing dendritic-like microglia expressing insulin-like growth factor 1. Proc Natl Acad Sci U S A 2006;103:11784-11789.
51. Oddo S, Caccamo A, Tseng B et al. Blocking Abeta42 accumulation delays the onset and progression of tau pathology via the C terminus of heat shock protein70-interacting protein: A mechanistic link between Abeta and tau pathology. J Neurosci 2008;28:12163-12175.
52. Oddo S, Caccamo A, Smith IF et al. Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A Link Between Abeta And Tau Pathology J Biol Chem 2006;281: 1599-1604.
53. Chen G, Chen KS, Knox J et al. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 2000;408:975-979.
54. Schindowski K, Bretteville A, Leroy K et al. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am J Pathol 2006;169:599-616.
55. Morris RG, Garrud P, Rawlins JN et al. Place navigation impaired in rats with hippocampal lesion. Nature 1982;297:681-683.
56. Parr AM, Tator CH, Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 2007;40:609-619.
57. Prockop DJ. "Stemness" does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clin Pharmacol Ther 2007;82:241-243.
58. Munoz JR, Stoutenger BR, Robinson AP et al. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 2005;102:18171-18176.
59. Bae JS, Han HS, Youn DH et al. Bone marrow-derived mesenchymal stem cells promote neuronal networks with functional synaptic transmission after transplantation into mice with neurodegeneration. Stem Cells 2007;25:1307-1316.