BMP9 ameliorates amyloidosis and the cholinergic defect in a mouse model of Alzheimer's disease

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 48, 2013, Pages 19567-19572

  Burke, Rebecca M ^a   Norman, Timothy A ^a   Haydar, Tarik F ^a   Slack, Barbara E ^a   Leeman, Susan E ^a   Blusztajn, Jan Krzysztof ^a   Mellott, Tiffany J ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine; APPswe PS1dE9 mice; Growth differentiation factor 2; Juvenile protective factors

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN[1-42]; BONE MORPHOGENETIC PROTEIN 9; CHOLINE ACETYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN 3; PROTEIN P75; PROTEIN TYROSINE KINASE A; SOMATOMEDIN C;

ALZHEIMER DISEASE; AMYLOID PLAQUE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CHOLINERGIC NERVE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FEMALE; FOREBRAIN; GENOTYPE; HIPPOCAMPUS; IMMUNOBLOTTING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; STRIATE CORTEX; WILD TYPE;

ACETYLCHOLINE; APPSWE PS1DE9 MICE; GROWTH/DIFFERENTIATION FACTOR 2; JUVENILE PROTECTIVE FACTORS;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANALYSIS OF VARIANCE; ANIMALS; CHOLINERGIC NEURONS; FEMALE; GROWTH DIFFERENTIATION FACTOR 2; IMMUNOASSAY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICROSCOPY, FLUORESCENCE;

EID: 84888338639     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1319297110     Document Type: Article

References (65)

1. Hasselmo ME, Sarter M (2011) Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36(1): 52-73.
2. López-Coviella I, Berse B, Krauss R, Thies RS, Blusztajn JK (2000) Induction and maintenance of the neuronal cholinergic phenotype in the central nervous system by BMP-9. Science 289(5477): 313-316.
3. Lopez-Coviella I, Mellott TJ, Schnitzler AC, Blusztajn JK (2011) BMP9 protects septal neurons from axotomy-evoked loss of cholinergic phenotype. PLoS ONE 6(6):e21166.
4. Bissonnette CJ, et al. (2011) The controlled generation of functional basal forebrain cholinergic neurons from human embryonic stem cells. Stem Cells 29(5): 802-811.
5. Lopez-Coviella I, et al. (2005) Bone morphogenetic protein 9 induces the transcriptome of basal forebrain cholinergic neurons. Proc Natl Acad Sci USA 102(19): 6984-6989.
6. Mufson EJ, Counts SE, Perez SE, Ginsberg SD (2008) Cholinergic system during the progression of Alzheimer's disease: Therapeutic implications. Expert Rev Neurother 8(11): 1703-1718.
7. Grothe M, Heinsen H, Teipel SJ (2012) Atrophy of the cholinergic basal forebrain over the adult age range and in early stages of Alzheimer's disease. Biol Psychiatry 71(9): 805-813.
8. Perez SE, Dar S, Ikonomovic MD, DeKosky ST, Mufson EJ (2007) Cholinergic forebrain degeneration in the APPswe/PS1DeltaE9 transgenic mouse. Neurobiol Dis 28(1): 3-15.
9. Machová E, et al. (2010) Functional cholinergic damage develops with amyloid accumulation in young adult APPswe/PS1dE9 transgenic mice. Neurobiol Dis 38(1): 27-35.
10. Goto Y, et al. (2008) Impaired muscarinic regulation of excitatory synaptic transmission in the APPswe/PS1dE9 mouse model of Alzheimer's disease. Eur J Pharmacol 583(1): 84-91.
11. Nikolajsen GN, Jensen MS, West MJ (2011) Cholinergic axon length reduced by 300 meters in the brain of an Alzheimer mouse model. Neurobiol Aging 32(11): 1927-1931.
12. Savonenko A, et al. (2005) Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: Relationships to beta-amyloid deposition and neurotransmitter abnormalities. Neurobiol Dis 18(3): 602-617.
13. Girão da Cruz MT, et al. (2012) Early increases in soluble amyloid-β levels coincide with cholinergic degeneration in 3xTg-AD mice. J Alzheimers Dis 32(2): 267-272.
14. Haense C, et al. (2012) Cholinergic system function and cognition in mild cognitive impairment. Neurobiol Aging 33(5): 867-877.
15. Howard R, et al. (2012) Donepezil and memantine for moderate-to-severe Alzheimer's disease. N Engl J Med 366(10): 893-903.
16. Terry RD, et al. (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 30(4): 572-580.
17. Sheng M, Sabatini BL, Südhof TC (2012) Synapses and Alzheimer's disease. Cold Spring Harb Perspect Biol 4(5):a005777.
18. Tuszynski MH, et al. (2005) A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11(5): 551-555.
19. Jankowsky JL, et al. (2001) Co-expression of multiple transgenes in mouse CNS: A comparison of strategies. Biomol Eng 17(6): 157-165.
20. Götz J, Ittner LM (2008) Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci 9(7): 532-544.
21. Jankowsky JL, et al. (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: Evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13(2): 159-170.
22. Park JH, et al. (2006) Subcutaneous Nogo receptor removes brain amyloid-beta and improves spatial memory in Alzheimer's transgenicmice. J Neurosci 26(51): 13279-13286.
23. O'Leary TP, Brown RE (2009) Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behav Brain Res 201(1): 120-127.
24. Gimbel DA, et al. (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 30(18): 6367-6374.
25. Kilgore M, et al. (2010) Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35(4): 870-880.
26. Kemppainen S, et al. (2012) Impaired TrkB receptor signaling contributes to memory impairment in APP/PS1 mice. Neurobiol Aging 33(6):1122.e1123-1139.
27. Garcia-Alloza M, et al. (2006) Characterization of amyloid deposition in the APPswe/ PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24(3): 516-524.
28. Tallini YN, et al. (2006) BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol Genomics 27(3): 391-397.
29. Schnitzler AC, et al. (2010) BMP9 (bone morphogenetic protein 9) induces NGF as an autocrine/paracrine cholinergic trophic factor in developing basal forebrain neurons. J Neurosci 30(24): 8221-8228.
30. Wang J, Tanila H, Puoliväli J, Kadish I, van Groen T (2003) Gender differences in the amount and deposition of amyloidbeta in APPswe and PS1 double transgenic mice. Neurobiol Dis 14(3): 318-327.
31. Hu L, Wong TP, Côté SL, Bell KF, Cuello AC (2003) The impact of Abeta-plaques on cortical cholinergic and non-cholinergic presynaptic boutons in Alzheimer's diseaselike transgenic mice. Neuroscience 121(2): 421-432.
32. Li Y, et al. (1995) Regulation of TrkA and ChAT expression in developing rat basal forebrain: Evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J Neurosci 15(4): 2888-2905.
33. Holtzman DM, et al. (1992) p140trk mRNA marks NGF-responsive forebrain neurons: Evidence that trk gene expression is induced by NGF. Neuron 9(3): 465-478.
34. Dawbarn D, Allen SJ, Semenenko FM (1988) Coexistence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain. Neurosci Lett 94(1-2): 138-144.
35. Woolf NJ, Gould E, Butcher LL (1989) Nerve growth factor receptor is associated with cholinergic neurons of the basal forebrain but not the pontomesencephalon. Neuroscience 30(1): 143-152.
36. Batchelor PE, Armstrong DM, Blaker SN, Gage FH (1989) Nerve growth factor receptor and choline acetyltransferase colocalization in neurons within the rat forebrain: Response to fimbria-fornix transection. J Comp Neurol 284(2): 187-204.
37. Kamphuis W, Orre M, Kooijman L, Dahmen M, Hol EM (2012) Differential cell proliferation in the cortex of the APPswePS1dE9 Alzheimer's disease mouse model. Glia 60(4): 615-629.
38. Kamphuis W, et al. (2012) GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS ONE 7(8):e42823.
39. Nitsch RM, Slack BE, Wurtman RJ, Growdon JH (1992) Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258(5080): 304-307.
40. Medeiros R, et al. (2011) Loss of muscarinic M1 receptor exacerbates Alzheimer's disease-like pathology and cognitive decline. Am J Pathol 179(2): 980-991.
41. Ramos-Rodriguez JJ, et al. (2013) Rapid β-amyloid deposition and cognitive impairment after cholinergic denervation in APP/PS1 mice. J Neuropathol Exp Neurol 72(4): 272-285.
42. Laursen B, Mørk A, Plath N, Kristiansen U, Bastlund JF (2013) Cholinergic degeneration is associated with increased plaque deposition and cognitive impairment in APPswe/PS1dE9 mice. Behav Brain Res 240: 146-152.
43. Meyer-Luehmann M, et al. (2008) Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451(7179): 720-724.
44. Mandrekar-Colucci S, Karlo JC, Landreth GE (2012) Mechanisms underlying the rapid peroxisome proliferator-activated receptor-γ-mediated amyloid clearance and reversal of cognitive deficits in a murine model of Alzheimer's disease. J Neurosci 32(30): 10117-10128.
45. Wyss-Coray T, et al. (2001) TGF-β1 promotes microglial amyloid-β clearance and reduces plaque burden in transgenic mice. Nat Med 7(5): 612-618.
46. Maier M, et al. (2006) Short amyloid-beta (Abeta) immunogens reduce cerebral Abeta load and learning deficits in an Alzheimer's disease mouse model in the absence of an Abeta-specific cellular immune response. J Neurosci 26(18): 4717-4728.
47. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109(5): 1953-1961.
48. Townson SA, et al. (2012) Specificity and structure of a high affinity activin receptorlike kinase 1 (ALK1) signaling complex. J Biol Chem 287(33): 27313-27325.
49. Ricard N, et al. (2012) BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 119(25): 6162-6171.
50. Sagare AP, Bell RD, Zlokovic BV (2012) Neurovascular dysfunction and faulty amyloid beta-peptide clearance in Alzheimer disease. Cold Spring Harb Perspect Med 2(10):pii: a011452.
51. Schliebs R, Arendt T (2011) The cholinergic system in aging and neuronal degeneration. Behav Brain Res 221(2): 555-563.
52. Wang YJ, et al. (2011) p75NTR regulates Abeta deposition by increasing Abeta production but inhibiting Abeta aggregation with its extracellular domain. J Neurosci 31(6): 2292-2304.
53. Robertson RT, Baratta J, Yu J, Guthrie KM (2006) A role for neurotrophin-3 in targeting developing cholinergic axon projections to cerebral cortex. Neuroscience 143(2): 523-539.
54. Lesné S, et al. (2005) Akt-dependent expression of NAIP-1 protects neurons against amyloid-β toxicity. J Biol Chem 280(26): 24941-24947.
55. Duron E, et al. (2012) Insulin-like growth factor-I and insulin-like growth factor binding protein-3 in Alzheimer's disease. J Clin Endocrinol Metab 97(12): 4673-4681.
56. Poirier R, Fernandez AM, Torres-Aleman I, Metzger F (2012) Early brain amyloidosis in APP/PS1 mice with serum insulin-like growth factor-I deficiency. Neurosci Lett 509(2): 101-104.
57. Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8(12): 1390-1397.
58. Doré S, Kar S, Quirion R (1997) Insulin-like growth factor I protects and rescues hippocampal neurons against beta-amyloid- and human amylin-induced toxicity. Proc Natl Acad Sci USA 94(9): 4772-4777.
59. Su AI, et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101(16): 6062-6067.
60. Marques F, et al. (2011) Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS 8(1):10.
61. Lehtinen MK, et al. (2011) The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69(5): 893-905.
62. Crews L, et al. (2010) Increased BMP6 levels in the brains of Alzheimer's disease patients and APP transgenic mice are accompanied by impaired neurogenesis. J Neurosci 30(37): 12252-12262.
63. Li D, et al. (2008) Decreased hippocampal cell proliferation correlates with increased expression of BMP4 in the APPswe/PS1DeltaE9 mouse model of Alzheimer's disease. Hippocampus 18(7): 692-698.
64. Tang J, et al. (2009) Noggin and BMP4 co-modulate adult hippocampal neurogenesis in the APP(swe)/PS1(DeltaE9) transgenic mouse model of Alzheimer's disease. Biochem Biophys Res Commun 385(3): 341-345.
65. Bergeron E, et al. (2012) The evaluation of ectopic bone formation induced by delivery systems for bone morphogenetic protein-9 or its derived peptide. Tissue Eng Part A 18(3-4): 342-352.