Angiotensin-converting enzyme overexpression in myelomonocytes prevents Alzheimer's-like cognitive decline

Journal of Clinical Investigation

Volumn 124, Issue 3, 2014, Pages 1000-1012

  Bernstein, Kenneth E ^a   Koronyo, Yosef ^a   Salumbides, Brenda C ^a   Sheyn, Julia ^a   Pelissier, Lindsey ^a   Lopes, Dahabada H J ^a   Shah, Kandarp H ^a   Bernstein, Ellen A ^a   Fuchs, Dieu Trang ^a   Yu, Jeff J Y ^a   Pham, Michael ^a   Black, Keith L ^a   Shen, Xiao Z ^a   Fuchs, Sebastien ^a,b   Koronyo Hamaoui, Maya ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; HYDRALAZINE; RAMIPRIL;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BARNES MAZE TEST; BRAIN TISSUE; CELL INFILTRATION; COGNITION; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; IMMUNE RESPONSE; INFLAMMATORY CELL; MALE; MONOCYTE; MOUSE; MYELOMONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; ASTROCYTES; CELL MOVEMENT; CEREBRAL CORTEX; COGNITION; FEMALE; HUMANS; MACROPHAGES; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID CELLS; PEPTIDYL-DIPEPTIDASE A; PLAQUE, AMYLOID; RAMIPRIL; SOLUBILITY;

EID: 84896799922     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI66541     Document Type: Article

References (79)

1. Brookmeyer R, et al. National estimates of the prevalence of Alzheimer's disease in the United States. Alzheimers Dement. 2011;7(1):61-73.
2. Selkoe DJ. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis. 2001;3(1):75-80.
3. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 2002; 297(5580):353-356.
4. Rufenacht P, Guntert A, Bohrmann B, Ducret A, Dobeli H. Quantification of the Aβ peptide in Alzheimer's plaques by laser dissection microscopy combined with mass spectrometry. J Mass Spectrom. 2005;40(2):193-201.
5. Shankar GM, et al. Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med. 2008; 14(8):837-842.
6. Zhang H, Ma Q, Zhang YW, Xu H. Proteolytic processing of Alzheimer's β-amyloid precursor protein. J Neurochem. 2012;120(suppl 1):9-21.
7. Selkoe DJ. Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior. Behav Brain Res. 2008;192(1):106-113.
8. Akiyama H, et al. Inflammation and Alzheimer's disease. Neurobiol Aging. 2000;21(3):383-421.
9. Bales KR, Du Y, Holtzman D, Cordell B, Paul SM. Neuroinflammation and Alzheimer's disease: critical roles for cytokine/Aβ-induced glial activation, NF-κB, and apolipoprotein E. Neurobiol Aging. 2000; 21(3):427-432.
10. McGeer PL, McGeer EG. Local neuroinflammation and the progression of Alzheimer's disease. J Neurovirol. 2002;8(6):529-538.
11. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med. 2006;12(9):1005-1015.
12. Selkoe DJ. Normal and abnormal biology of the β-amyloid precursor protein. Annu Rev Neurosci. 1994;17:489-517.
13. Saido TC. Alzheimer's disease as proteolytic disorders: anabolism and catabolism of β-amyloid. Neurobiol Aging. 1998;19(1 suppl):S69-S75.
14. De Felice FG, Ferreira ST. Beta-amyloid production, aggregation, and clearance as targets for therapy in Alzheimer's disease. Cell Mol Neurobiol. 2002; 22(5-6):545-563.
15. Mawuenyega KG, et al. Decreased clearance of CNS β-amyloid in Alzheimer's disease. Science. 2010; 330(6012):1774.
16. Lee EB, et al. Targeting amyloid-β peptide (Abeta) oligomers by passive immunization with a conformation-selective monoclonal antibody improves learning and memory in Aβ precursor protein (APP) transgenic mice. J Biol Chem. 2006;281(7):4292-4299.
17. Nitsch RM, Hock C. Targeting β-amyloid pathology in Alzheimer's disease with Aβ immunotherapy. Neurotherapeutics. 2008;5(3):415-420.
18. Cho JE, Kim JR. Recent approaches targeting β-amyloid for therapeutic intervention of Alzheimer's disease. Recent Pat CNS Drug Discov. 2011; 6(3):222-233.
19. Bernstein KE, et al. A modern understanding of the traditional and nontraditional biological functions of angiotensin-converting enzyme. Pharmacol Rev. 2013;65(1):1-46.
20. Hemming ML, Selkoe DJ. Amyloid β-protein is degraded by cellular angiotensin-converting enzyme (ACE) and elevated by an ACE inhibitor. J Biol Chem. 2005;280(45):37644-37650.
21. Zou K, et al. Aβ42-to-Aβ40-and angiotensin-converting activities in different domains of angiotensin-converting enzyme. J Biol Chem. 2009; 284(46):31914-31920.
22. Zou K, et al. Angiotensin-converting enzyme converts amyloid β-protein 1-42 (Aβ(1-42)) to Aβ(1-40), and its inhibition enhances brain Aβ deposition. J Neurosci. 2007;27(32):8628-8635.
23. Harmer D, Gilbert M, Borman R, Clark KL. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 2002;532(1-2):107-110.
24. Shen XZ, et al. Mice with enhanced macrophage angiotensin-converting enzyme are resistant to melanoma. Am J Pathol. 2007;170(6):2122-2134.
25. Okwan-Duodu D, et al. Angiotensin-converting enzyme overexpression in mouse myelomonocytic cells augments resistance to Listeria and methicillin-resistant Staphylococcus aureus. J Biol Chem. 2010;285(50):39051- 39060.
26. Shen XZ, et al. The carboxypeptidase ACE shapes the MHC class I peptide repertoire. Nat Immunol. 2011;12(11):1078-1085.
27. Colton CA, Chernyshev ON, Gilbert DL, Vitek MP. Microglial contribution to oxidative stress in Alzheimer's disease. Ann N Y Acad Sci. 2000; 899:292-307.
28. D'Andrea MR, Cole GM, Ard MD. The microglial phagocytic role with specific plaque types in the Alzheimer disease brain. Neurobiol Aging. 2004; 25(5):675-683.
29. Malm TM, et al. Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to β-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol Dis. 2005; 18(1):134-142.
30. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron. 2006;49(4):489-502.
31. Butovsky O, Kunis G, Koronyo-Hamaoui M, Schwartz M. Selective ablation of bone marrow-derived dendritic cells increases amyloid plaques in a mouse Alzheimer's disease model. Eur J Neurosci. 2007;26(2):413-416.
32. Fiala M, Cribbs DH, Rosenthal M, Bernard G. Phagocytosis of amyloid-β and inflammation: two faces of innate immunity in Alzheimer's disease. J Alzheimers Dis. 2007;11(4):457-463.
33. Cameron B, Landreth GE. Inflammation, microglia, and Alzheimer's disease. Neurobiol Dis. 2010; 37(3):503-509.
34. Lai AY, McLaurin J. Clearance of amyloid-β peptides by microglia and macrophages: the issue of what, when and where. Future Neurol. 2012; 7(2):165-176.
35. Mizuno T. The biphasic role of microglia in Alzheimer's disease. Int J Alzheimers Dis. 2012; 2012:737846.
36. Koronyo-Hamaoui M, et al. Attenuation of ADlike neuropathology by harnessing peripheral immune cells: local elevation of IL-10 and MMP-9. J Neurochem. 2009;111(6):1409-1424.
37. Simard AR, Rivest S. Neuroprotective properties of the innate immune system and bone marrow stem cells in Alzheimer's disease. Mol Psychiatry. 2006; 11(4):327-335.
38. El Khoury J, et al. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med. 2007;13(4):432-438.
39. Schwartz M, Shechter R. Systemic inflammatory cells fight off neurodegenerative disease. Nat Rev Neurol. 2010;6(7):405-410.
40. Lebson L, et al. Trafficking CD11b-positive blood cells deliver therapeutic genes to the brain of amyloid-depositing transgenic mice. J Neurosci. 2010; 30(29):9651-9658.
41. Hickman SE, El Khoury J. Mechanisms of mononuclear phagocyte recruitment in Alzheimer's disease. CNS Neurol Disord Drug Targets. 2010;9(2):168-173.
42. Jankowsky JL, et al. 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. 2004; 13(2):159-170.
43. Chakrabarty P, et al. IFN-γ promotes complement expression and attenuates amyloid plaque deposition in amyloid beta precursor protein transgenic mice. J Immunol. 2010;184(9):5333-5343.
44. Garcia-Alloza M, et al. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis. 2006;24(3):516-524.
45. Miao J, et al. Reducing cerebral microvascular amyloid-β protein deposition diminishes regional neuroinflammation in vasculotropic mutant amyloid precursor protein transgenic mice. J Neurosci. 2005;25(27):6271-6277.
46. Akiyama H, et al. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis Assoc Disord. 2000;14(suppl 1):S47-S53.
47. Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease - a double-edged sword. Neuron. 2002;35(3):419-432.
48. Gohlke P, Scholkens B, Henning R, Urbach H, Unger T. Inhibition of converting enzyme in brain tissue and cerebrospinal fluid of rats following chronic oral treatment with the converting enzyme inhibitors ramipril and Hoe 22. J Cardiovasc Pharmacol. 1989;14(Suppl 4):S32-S36
49. Prinz M, Priller J, Sisodia SS, Ransohoff RM. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci. 2011; 14(10):1227-1235.
50. Savino B, et al. Control of murine Ly6C(high) monocyte traffic and immunosuppressive activities by atypical chemokine receptor D6. Blood. 2012; 119(22):5250-5260.
51. Marques CP, et al. Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol. 2008; 181(9):6417-6426.
52. Wohleb ES, et al. β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci. 2011;31(17):6277-6288.
53. Juedes AE, Ruddle NH. Resident and infiltrating central nervous system APCs regulate the emergence and resolution of experimental autoimmune encephalomyelitis. J Immunol. 2001;166(8):5168-5175.
54. O'Leary TP, Brown RE. 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. 2009; 201(1):120-127.
55. Reiserer RS, Harrison FE, Syverud DC, McDonald MP. Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav. 2007;6(1):54-65.
56. Walker JM, et al. Spatial learning and memory impairment and increased locomotion in a transgenic amyloid precursor protein mouse model of Alzheimer's disease. Behav Brain Res. 2011; 222(1):169-175.
57. Shen XZ, et al. Nontraditional roles of angiotensin-converting enzyme. Hypertension. 2012; 59(4):763-768.
58. Boissonneault V, et al. Powerful beneficial effects of macrophage colony-stimulating factor on β-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain. 2009;132(pt 4):1078-1092.
59. Paresce DM, Ghosh RN, Maxfield FR. Microglial cells internalize aggregates of the Alzheimer's disease amyloid β-protein via a scavenger receptor. Neuron. 1996;17(3):553-565.
60. Webster SD, et al. Complement component C1q modulates the phagocytosis of Aβ by microglia. Exp Neurol. 2000;161(1):127-138.
61. Bakalash S, et al. Egr1 expression is induced following glatiramer acetate immunotherapy in rodent models of glaucoma and Alzheimer's disease. Invest Ophthalmol Vis Sci. 2011;52(12):9033-9046.
62. Butovsky O, 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(31):11784-11789
63. Sun X, et al. Catabolic attacks of membrane-bound angiotensin-converting enzyme on the N-terminal part of species-specific amyloid-β peptides. Eur J Pharmacol. 2008;588(1):18-25.
64. Kehoe PG, Miners S, Love S. Angiotensins in Alzheimer's disease - friend or foe? Trends Neurosci. 2009;32(12):619-628.
65. Kehoe PG. Angiotensins and Alzheimer's disease: a bench to bedside overview. Alzheimers Res Ther. 2009;1(1):3.
66. Miners JS, et al. Angiotensin-converting enzyme (ACE) levels and activity in Alzheimer's disease, and relationship of perivascular ACE-1 to cerebral amyloid angiopathy. Neuropathol Appl Neurobiol. 2008; 34(2):181-193.
67. Hemming ML, Selkoe DJ, Farris W. Effects of prolonged angiotensin-converting enzyme inhibitor treatment on amyloid β-protein metabolism in mouse models of Alzheimer disease. Neurobiol Dis. 2007;26(1):273-281.
68. Kehoe PG, et al. Common variants of ACE contribute to variable age-at-onset of Alzheimer's disease. Hum Genet. 2004;114(5):478-483.
69. Kolsch H, et al. ACE I/D polymorphism is a risk factor of Alzheimer's disease but not of vascular dementia. Neurosci Lett. 2005;377(1):37-39.
70. Lehmann DJ, et al. Large meta-analysis establishes the ACE insertion-deletion polymorphism as a marker of Alzheimer's disease. Am J Epidemiol. 2005; 162(4):305-317.
71. Narain Y, et al. The ACE gene and Alzheimer's disease susceptibility. J Med Genet. 2000;37(9):695-697.
72. Lendon CL, et al. The angiotensin 1-converting enzyme insertion (I)/deletion (D) polymorphism does not influence the extent of amyloid or tau pathology in patients with sporadic Alzheimer's disease. Neurosci Lett. 2002;328(3):314-318.
73. Kehoe PG, Passmore PA. The renin-angiotensin system and antihypertensive drugs in Alzheimer's disease: current standing of the angiotensin hypothesis? J Alzheimers Dis. 2012; 30(suppl 2):S251-S268.
74. Jankowsky JL, et al. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng. 2001;17(6):157-165.
75. Cole J, et al. Mice lacking endothelial angiotensinconverting enzyme have a normal blood pressure. Circ Res. 2002;90(1):87-92.
76. Langford KG, et al. Transgenic mice demonstrate a testis-specific promoter for angiotensin-converting enzyme. J Biol Chem. 1991; 266(24):15559-15562.
77. Koronyo-Hamaoui M, et al. Identification of amyloid plaques in retinas from Alzheimer's patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage. 2011; 54(suppl 1):S204-S217.
78. Fuchs S, et al. Role of the N-terminal catalytic domain of angiotensin-converting enzyme investigated by targeted inactivation in mice. J Biol Chem. 2004;279(16):15946-15953.
79. Pechnick RN, et al. Developmental exposure to corticosterone: behavioral changes and differential effects on leukemia inhibitory factor (LIF) and corticotropin-releasing hormone (CRH) gene expression in the mouse. Psychopharmacology (Berl). 2006; 185(1):76-83.