Microrna-33 regulates apoe lipidation and amyloid-β metabolism in the brain

Journal of Neuroscience

Volumn 35, Issue 44, 2015, Pages 14717-14726

  Kim, Jaekwang ^a,b   Yoon, Hyejin ^a,b   Horie, Takahiro ^c   Burchett, Jack M ^b   Restivo, Jessica L ^b   Rotllan, Noemi ^d   Ramírez, Cristina M ^d   Verghese, Philip B ^b   Ihara, Masafumi ^e   Hoe, Hyang Sook ^f   Esau, Christine ^g   Fernández Hernando, Carlos ^d   Holtzman, David M ^b   Cirrito, John R ^b   Ono, Koh ^c   Kim, Jungsu ^a,b  

^a MAYO CLINIC   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^f GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^g REGULUS THERAPEUTICS   (United States)

Author keywords

ABCA1; Abeta; Alzheimer s disease; ApoE; MiR 33

Indexed keywords

ABC TRANSPORTER A1; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; MICRORNA; MICRORNA 33; UNCLASSIFIED DRUG; MIRN33 MICRORNA, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE SEQUENCE; LIPID METABOLISM; LUCIFERASE ASSAY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; TRANSGENIC MOUSE;

AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BASE SEQUENCE; BRAIN; HUMANS; LIPID METABOLISM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICRORNAS; MOLECULAR SEQUENCE DATA;

EID: 84946429411     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2053-15.2015     Document Type: Article

References (41)

1. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29:341-345. CrossRef Medline
2. Bien-Ly N, Gillespie AK, Walker D, Yoon SY, Huang Y (2012) Reducing human apolipoprotein E levels attenuates age-dependent Abeta accumulation in mutant human amyloid precursor protein transgenic mice. J Neurosci 32:4803-4811. CrossRef Medline
3. Di Paolo G, Kim TW (2011) Linking lipids to Alzheimer’s disease: cholesterol and beyond. Nat Rev Neurosci 12:284-296. CrossRef Medline
4. Ebert MS, Sharp PA (2012) Roles for microRNAs in conferring robustness to biological processes. Cell 149:515-524. CrossRef Medline
5. Faravelli I, Nizzardo M, Comi GP, Corti S (2015) Spinal muscular atrophy: recent therapeutic advances for an old challenge. Nat Rev Neurol 11:351-359. CrossRef Medline
6. Gaudet D, Alexander VJ, Baker BF, Brisson D, Tremblay K, Singleton W, Geary RS, Hughes SG, Viney NJ, Graham MJ, Crooke RM, Witztum JL, Brunzell JD, Kastelein JJ (2015) Antisense inhibition of apolipoprotein C-III in patients with hypertriglyceridemia. N Engl J Med 373:438-447. CrossRef Medline
7. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide. Nat Rev Mol Cell Biol 8:101-112. CrossRef Medline
8. Hebert SS, Horre´ K, Nicolaï L, Bergmans B, Papadopoulou AS, Delacourte A, De Strooper B (2009) MicroRNA regulation of Alzheimer’s amyloid precursor protein expression. Neurobiol Dis 33:422-428. CrossRef Medline
9. Hirsch-Reinshagen V, Zhou S, Burgess BL, Bernier L, McIsaac SA, Chan JY, Tansley GH, Cohn JS, Hayden MR, Wellington CL (2004) Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J Biol Chem 279: 41197-41207. CrossRef Medline
10. Horie T, Ono K, Horiguchi M, Nishi H, Nakamura T, Nagao K, Kinoshita M, Kuwabara Y, Marusawa H, Iwanaga Y, Hasegawa K, Yokode M, Kimura T, Kita T (2010) MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulatesHDLin vivo. Proc Natl Acad Sci U S A 107:17321-17326. CrossRef Medline
11. 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 beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13:159-170. CrossRef Medline
12. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58:681-693. CrossRef Medline
13. Jovicˇic´ A, Roshan R, Moisoi N, Pradervand S, Moser R, Pillai B, Luthi-Carter R (2013) Comprehensive expression analyses of neural cell-typespecific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 33:5127-5137. CrossRef Medline
14. Kanasty R, Dorkin JR, Vegas A, Anderson D (2013) Delivery materials for siRNA therapeutics. Nat Mater 12:967-977. CrossRef Medline
15. Kim J, Miller VM, Levites Y, West KJ, Zwizinski CW, Moore BD, Troendle FJ, Bann M, Verbeeck C, Price RW, Smithson L, Sonoda L, Wagg K, Rangachari V, Zou F, Younkin SG, Graff-Radford N, Dickson D, Rosenberry T, Golde TE (2008) BRI2 (ITM2b) inhibits Abeta deposition in vivo. J Neurosci 28:6030-6036. CrossRef Medline
16. Kim J, Basak JM, Holtzman DM (2009a) The role of apolipoprotein E in Alzheimer’s disease. Neuron 63:287-303. CrossRef Medline
17. Kim J, Castellano JM, Jiang H, Basak JM, Parsadanian M, Pham V, Mason SM, Paul SM, Holtzman DM (2009b) Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular A beta clearance. Neuron 64:632-644. CrossRef Medline
18. Kim J, Yoon H, Ramírez CM, Lee SM, Hoe HS, Fernández-Hernando C, Kim J (2012) MiR-106b impairs cholesterol efflux and increases Abeta levels by repressing ABCA1 expression. Exp Neurol 235:476-483. CrossRef Medline
19. Kim WS, Rahmanto AS, Kamili A, Rye KA, Guillemin GJ, Gelissen IC, Jessup W, Hill AF, Garner B (2007) Role of ABCG1 and ABCA1 in regulation of neuronal cholesterol efflux to apolipoprotein E discs and suppression of amyloid-beta peptide generation. J Biol Chem 282:2851-2861. CrossRef Medline
20. Koldamova RP, Lefterov IM, Ikonomovic MD, Skoko J, Lefterov PI, Isanski BA, DeKosky ST, Lazo JS (2003) 22R-hydroxycholesterol and 9-cisretinoic acid induce ATP-binding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid beta secretion. J Biol Chem 278:13244-13256. CrossRef Medline
21. Koldamova R, Staufenbiel M, Lefterov I (2005) Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. J Biol Chem 280:43224-43235. CrossRef Medline
22. Koldamova R, Fitz NF, Lefterov I (2010) The role of ATP-binding cassette transporter A1 in Alzheimer’s disease and neurodegeneration. Biochim Biophys Acta 1801:824-830. CrossRef Medline
23. Koldamova R, Fitz NF, Lefterov I (2014) ATP-binding cassette transporter A1: from metabolism to neurodegeneration. Neurobiol Dis 72:13-21. CrossRef Medline
24. Kumar P, Wu H, McBride JL, Jung KE, Kim MH, Davidson BL, Lee SK, Shankar P, Manjunath N (2007) Transvascular delivery of small interfering RNA to the central nervous system. Nature 448:39-43. CrossRef Medline
25. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foa R, Schliwka J, Fuchs U, Novosel A, Müller RU, et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414. CrossRef Medline
26. Mendell JT, Olson EN (2012) MicroRNAs in stress signaling and human disease. Cell 148:1172-1187. CrossRef Medline
27. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, Näär AM (2010) MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 328:1566-1569. CrossRef Medline
28. Nelson PT, Keller JN (2007) RNA in brain disease: no longer just “the messenger in the middle.” J Neuropathol Exp Neurol 66:461-468.
29. Pulford B, Reim N, Bell A, Veatch J, Forster G, Bender H, Meyerett C, Hafeman S, Michel B, Johnson T, Wyckoff AC, Miele G, Julius C, Kranich J, Schenkel A, Dow S, Zabel MD (2010) Liposome-siRNA-peptide complexes cross the blood-brain barrier and significantly decrease PrP on neuronal cells and PrP in infected cell cultures. PLoS One 5:e11085. CrossRef Medline
30. Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernández-Hernando C (2010) MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328:1570-1573. CrossRef Medline
31. Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, Parathath S, van Gils JM, Rayner AJ, Chang AN, Suarez Y, Fernandez-Hernando C, Fisher EA, Moore KJ (2011a) Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 121: 2921-2931. CrossRef Medline
32. Rayner KJ, Esau CC, Hussain FN, McDaniel AL, Marshall SM, van Gils JM, Ray TD, Sheedy FJ, Goedeke L, Liu X, Khatsenko OG, Kaimal V, Lees CJ, Fernandez-Hernando C, Fisher EA, Temel RE, Moore KJ (2011b) Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 478:404-407. CrossRef Medline
33. Rigo F, Chun SJ, Norris DA, Hung G, Lee S, Matson J, Fey RA, Gaus H, Hua Y, Grundy JS, Krainer AR, Henry SP, Bennett CF (2014) Pharmacology of a central nervous system delivered 2β-O-methoxyethyl-modified survival of motor neuron splicing oligonucleotide in mice and nonhuman primates. J Pharmacol Exp Ther 350:46-55. CrossRef Medline
34. Roshan R, Shridhar S, Sarangdhar MA, Banik A, Chawla M, Garg M, Singh VP, Pillai B (2014) Brain-specific knockdown of miR-29 results in neuronal cell death and ataxia in mice. RNA20:1287-1297. CrossRef Medline
35. Rottiers V, Obad S, Petri A, McGarrah R, Lindholm MW, Black JC, Sinha S, Goody RJ, Lawrence MS, deLemos AS, Hansen HF, Whittaker S, Henry S, Brookes R, Najafi-Shoushtari SH, Chung RT, Whetstine JR, Gerszten RE, Kauppinen S, Näär AM (2013) Pharmacological inhibition of a microRNA family in nonhuman primates by a seed-targeting 8-mer antimiR. Sci Transl Med 5:212. CrossRef Medline
36. Sun Y, Yao J, Kim TW, Tall AR (2003) Expression of liver X receptor target genes decreases cellular amyloid beta peptide secretion. J Biol Chem 278: 27688-27694. CrossRef Medline
37. van Rooij E, Kauppinen S (2014) Development of microRNA therapeutics is coming of age. EMBO Mol Med 6:851-864. CrossRef Medline
38. Velagapudi SP, Vummidi BR, Disney MD (2015) Small molecule chemical probes of microRNA function. Curr Opin Chem Biol 24:97-103. CrossRef Medline
39. Wahrle SE, Jiang H, Parsadanian M, Legleiter J, Han X, Fryer JD, Kowalewski T, Holtzman DM (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. J Biol Chem 279:40987-40993. CrossRef Medline
40. Wahrle SE, Jiang H, Parsadanian M, Hartman RE, Bales KR, Paul SM, Holtzman DM (2005) Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J Biol Chem 280: 43236-43242. CrossRef Medline
41. Wahrle SE, Jiang H, Parsadanian M, Kim J, Li A, Knoten A, Jain S, Hirsch-Reinshagen V, Wellington CL, Bales KR, Paul SM, Holtzman DM (2008) Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J Clin Invest 118:671-682. CrossRef Medline