Intravenously injected human apolipoprotein A-I rapidly enters the central nervous system via the choroid plexus

Journal of the American Heart Association

Volumn 3, Issue 6, 2014, Pages

  Stukas, Sophie ^a   Robert, Jerome ^a   Lee, Michael ^a   Kulic, Iva ^a   Carr, Michael ^a   Tourigny, Katherine ^a   Fan, Jianjia ^a   Namjoshi, Dhananjay ^a   Lemke, Kalistyne ^b   DeValle, Nicole ^b   Chan, Jeniffer ^a   Wilson, Tammy ^a   Wilkinson, Anna ^a   Chapanian, Rafi ^a   Kizhakkedathu, Jayachandran N ^a   Cirrito, John R ^c   Oda, Michael N ^b   Wellington, Cheryl L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ApoA I; Central nervous system; Cerebrovascular endothelium; Choroid plexus; Transport

Indexed keywords

APOLIPOPROTEIN A1; EVANS BLUE; MESSENGER RNA; APOA1 PROTEIN, HUMAN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; INTERNALIZATION; INTERSTITIAL FLUID; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; STEADY STATE; ANIMAL; BLOOD; BLOOD BRAIN BARRIER; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL CULTURE; GENETICS; HALF LIFE TIME; INTRAVENOUS DRUG ADMINISTRATION; KNOCKOUT MOUSE; METABOLIC CLEARANCE RATE; METABOLISM; TISSUE DISTRIBUTION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOLIPOPROTEIN A-I; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CELLS, CULTURED; CHOROID PLEXUS; ENDOTHELIAL CELLS; EPITHELIAL CELLS; FEMALE; HALF-LIFE; HUMANS; INJECTIONS, INTRAVENOUS; METABOLIC CLEARANCE RATE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT PROTEINS; TISSUE DISTRIBUTION;

EID: 84924167024     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.001156     Document Type: Article

References (59)

1. Shah AS, Tan L, Long JL, Davidson WS. Proteomic diversity of high density lipoproteins: our emerging understanding of its importance in lipid transport and beyond. J Lipid Res. 2013;54:2575-2585.
2. Kontush A, Lhomme M, Chapman MJ. Unraveling the complexities of the HDL lipidome. J Lipid Res. 2013;54:2950-2963.
3. Mineo C, Shaul PW. Novel biological functions of high-density lipoprotein cholesterol. Circ Res. 2012;111:1079-1090.
4. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci. 2011;12:723-738.
5. Stukas S, Robert J, Wellington CL. High density lipoproteins and cerebrovasular integrity in Alzheimer's disease. Cell Metab. 2014;19:574-591.
6. Mayeux R, Stern Y. Epidemiology of Alzheimer disease. Cold Spring Harb Perspect Med. 2012;2:a006239.
7. Duron E, Hanon O. Vascular risk factors, cognitive decline, and dementia. Vasc Health Risk Manag. 2008;4:363-381.
8. Sorrentino SA, Besler C, Rohrer L, Meyer M, Heinrich K, Bahlmann FH, Mueller M, Horvath T, Doerries C, Heinemann M, Flemmer S, Markowski A, Manes C, Bahr MJ, Haller H, von Eckardstein A, Drexler H, Landmesser U. Endothelialvasoprotective effects of high-density lipoprotein are impaired in patients with type 2 diabetes mellitus but are improved after extended-release niacin therapy. Circulation. 2010;121:110-122.
9. Riwanto M, Rohrer L, Roschitzki B, Besler C, Mocharla P, Mueller M, Perisa D, Heinrich K, Altwegg L, von Eckardstein A, Luscher TF, Landmesser U. Altered activation of endothelial anti-and proapoptotic pathways by high-density lipoprotein from patients with coronary artery disease: role of high-density lipoprotein-proteome remodeling. Circulation. 2013;127:891-904.
10. Lefterov I, Fitz NF, Cronican AA, Fogg A, Lefterov P, Kodali R, Wetzel R, Koldamova R. Apolipoprotein A-I deficiency increases cerebral amyloid angiopathy and cognitive deficits in APP/PS1DeltaE9 mice. J Biol Chem. 2010;285:36945-36957.
11. Lewis TL, Cao D, Lu H, Mans RA, Su YR, Jungbauer L, Linton MF, Fazio S, LaDu MJ, Li L. Overexpression of human apolipoprotein A-I preserves cognitive function and attenuates neuroinflammation and cerebral amyloid angiopathy in a mouse model of Alzheimer disease. J Biol Chem. 2010;285:36958-36968.
12. Paula-Lima AC, Tricerri MA, Brito-Moreira J, Bomfim TR, Oliveira FF, Magdesian MH, Grinberg LT, Panizzutti R, Ferreira ST. Human apolipoprotein A-I binds amyloid-beta and prevents Abeta-induced neurotoxicity. Int J Biochem Cell Biol. 2009;41:1361-1370.
13. Hirsch-Reinshagen V, Zhou S, Burgess BL, Bernier L, McIsaac SA, Chan JY, Tansley GH, Cohn JS, Hayden MR, Wellington CL. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J Biol Chem. 2004;279:41197-41207.
14. Stukas S, May S, Wilkinson A, Chan J, Donkin J, Wellington CL. The LXR agonist GW3965 increases apoA-I protein levels in the central nervous system independent of ABCA1. Biochim Biophys Acta. 2012;1821:536-546.
15. Karasinska JM, Rinninger F, Lutjohann D, Ruddle P, Franciosi S, Kruit JK, Singaraja RR, Hirsch-Reinshagen V, Fan J, Brunham LR, Bissada N, Ramakrishnan R, Wellington CL, Parks JS, Hayden MR. Specific loss of brain ABCA1 increases brain cholesterol uptake and influences neuronal structure and function. J Neurosci. 2009;29:3579-3589.
16. 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. Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J Clin Invest. 2008;118:671-682.
17. Mockel B, Zinke H, Flach R, Weiss B, Weiler-Guttler H, Gassen HG. Expression of apolipoprotein A-I in porcine brain endothelium in vitro. J Neurochem. 1994;62:788-798.
18. Ulrich JD, Burchett JM, Restivo JL, Schuler DR, Verghese PB, Mahan TE, Landreth GE, Castellano JM, Jiang H, Cirrito JR, Holtzman DM. In vivo measurement of apolipoprotein e from the brain interstitial fluid using microdialysis. Mol Neurodegener. 2013;8:13.
19. Cirrito JR, May PC, O'Dell MA, Taylor JW, Parsadanian M, Cramer JW, Audia JE, Nissen JS, Bales KR, Paul SM, DeMattos RB, Holtzman DM. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. J Neurosci. 2003;23:8844-8853.
20. Robert J, Weber B, Frese L, Emmert MY, Schmidt D, von Eckardstein A, Rohrer L, Hoerstrup SP. A three-dimensional engineered artery model for in vitro atherosclerosis research. PLoS One. 2013;8:e79821.
21. Rohrer L, Cavelier C, Fuchs S, Schluter MA, Volker W, von Eckardstein A. Binding, internalization and transport of apolipoprotein A-I by vascular endothelial cells. Biochim Biophys Acta. 2006;1761:186-194.
22. Strazielle N, Ghersi-Egea JF. Physiology of blood-brain interfaces in relation to brain disposition of small compounds and macromolecules. Mol Pharm. 2013;10:1473-1491.
23. Kratzer I, Wernig K, Panzenboeck U, Bernhart E, Reicher H, Wronski R, Windisch M, Hammer A, Malle E, Zimmer A, Sattler W. Apolipoprotein A-I coating of protamine-oligonucleotide nanoparticles increases particle uptake and transcytosis in an in vitro model of the blood-brain barrier. J Control Release. 2007;117:301-311.
24. Walter M. Interrelationships among HDL metabolism, aging, and atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:1244-1250.
25. Saczynski JS, White L, Peila RL, Rodriguez BL, Launer LJ. The relation between apolipoprotein A-I and dementia: the Honolulu-Asia aging study. Am J Epidemiol. 2007;165:985-992.
26. Reitz C, Tang MX, Schupf N, Manly JJ, Mayeux R, Luchsinger JA. Association of higher levels of high-density lipoprotein cholesterol in elderly individuals and lower risk of late-onset Alzheimer disease. Arch Neurol. 2010;67:1491-1497.
27. Kawano M, Kawakami M, Otsuka M, Yashima H, Yaginuma T, Ueki A. Marked decrease of plasma apolipoprotein AI and AII in Japanese patients with lateonset non-familial Alzheimer's disease. Clin Chim Acta. 1995;239:209-211.
28. Kuriyama M, Takahashi K, Yamano T, Hokezu Y, Togo S, Osame M, Igakura T. Low levels of serum apolipoprotein A I and A II in senile dementia. Jpn J Psychiatry Neurol. 1994;48:589-593.
29. Merched A, Xia Y, Visvikis S, Serot JM, Siest G. Decreased high-density lipoprotein cholesterol and serum apolipoprotein AI concentrations are highly correlated with the severity of Alzheimer's disease. Neurobiol Aging. 2000;21:27-30.
30. Shih YH, Tsai KJ, Lee CW, Shiesh SC, Chen WT, Pai MC, Kuo YM. Apolipoprotein C-III is an amyloid-beta-binding protein and an early marker for Alzheimer's disease. J Alzheimers Dis. 2014;41:855-865.
31. Hye A, Riddoch-Contreras J, Baird AL, Ashton NJ, Bazenet C, Leung R, Westman E, Simmons A, Dobson R, Sattlecker M, Lupton M, Lunnon K, Keohane A, Ward M, Pike I, Zucht HD, Pepin D, Zheng W, Tunnicliffe A, Richardson J, Gauthier S, Soininen H, Kloszewska I, Mecocci P, Tsolaki M, Vellas B, Lovestone S. Plasma proteins predict conversion to dementia from prodromal disease. Alzheimers Dement. 2014; epub ahead of print available online July 3 2014.
32. Reed B, Villeneuve S, Mack W, DeCarli C, Chui HC, Jagust W. Associations between serum cholesterol levels and cerebral amyloidosis. JAMA Neurol. 2014;71:195-200.
33. Puchades M, Hansson SF, Nilsson CL, Andreasen N, Blennow K, Davidsson P. Proteomic studies of potential cerebrospinal fluid protein markers for Alzheimer's disease. Brain Res Mol Brain Res. 2003;118:140-146.
34. Castano EM, Roher AE, Esh CL, Kokjohn TA, Beach T. Comparative proteomics of cerebrospinal fluid in neuropathologically-confirmed Alzheimer's disease and non-demented elderly subjects. Neurol Res. 2006;28:155-163.
35. Roher AE, Maarouf CL, Sue LI, Hu Y, Wilson J, Beach TG. Proteomics-derived cerebrospinal fluid markers of autopsy-confirmed Alzheimer's disease. Biomarkers. 2009;14:493-501.
36. Harr SD, Uint L, Hollister R, Hyman BT, Mendez AJ. Brain expression of apolipoproteins E, J, and A-I in Alzheimer's disease. J Neurochem. 1996;66:2429-2435.
37. Song H, Saito K, Seishima M, Noma A, Urakami K, Nakashima K. Cerebrospinal fluid apo E and apo A-I concentrations in early-and late-onset Alzheimer's disease. Neurosci Lett. 1997;231:175-178.
38. Balazs Z, Panzenboeck U, Hammer A, Sovic A, Quehenberger O, Malle E, Sattler W. Uptake and transport of high-density lipoprotein (HDL) and HDLassociated alpha-tocopherol by an in vitro blood-brain barrier model. J Neurochem. 2004;89:939-950.
39. Sovic A, Balazs Z, Hrzenjak A, Reicher H, Panzenboeck U, Malle E, Sattler W. Scavenger receptor class B, type I mediates uptake of lipoprotein-associated phosphatidylcholine by primary porcine cerebrovascular endothelial cells. Neurosci Lett. 2004;368:11-14.
40. Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu L, Wagner S, Buchel C, von Briesen H, Kreuter J. Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J Control Release. 2009;137:78-86.
41. Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu L, Buchel C, Kreuter J. Human serum albumin nanoparticles modified with apolipoprotein A-I cross the blood-brain barrier and enter the rodent brain. J Drug Target. 2010;18:842-848.
42. Kingwell BA, Chapman MJ, Kontush A, Miller NE. HDL-targeted therapies: progress, failures and future. Nat Rev Drug Discov. 2014;13:445-464.
43. Duvernoy HM, Risold PY. The circumventricular organs: an atlas of comparative anatomy and vascularization. Brain Res Rev. 2007;56: 119-147.
44. Langlet F, Mullier A, Bouret SG, Prevot V, Dehouck B. Tanycyte-like cells form a blood-cerebrospinal fluid barrier in the circumventricular organs of the mouse brain. J Comp Neurol. 2013;521:3389-3405.
45. Cavelier C, Rohrer L, von Eckardstein A. ATP-binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells. Circ Res. 2006;99:1060-1066.
46. Cavelier C, Ohnsorg PM, Rohrer L, von Eckardstein A. The beta-chain of cell surface F(0)F(1) atpase modulates apoa-I and HDL transcytosis through aortic endothelial cells. Arterioscler Thromb Vasc Biol. 2012;32:131-139.
47. Moestrup SK, Nielsen LB. The role of the kidney in lipid metabolism. Curr Opin Lipidol. 2005;16:301-306.
48. Assemat E, Chatelet F, Chandellier J, Commo F, Cases O, Verroust P, Kozyraki R. Overlapping expression patterns of the multiligand endocytic receptors cubilin and megalin in the CNS, sensory organs and developing epithelia of the rodent embryo. Gene Expr Patterns. 2005;6:69-78.
49. Carro E, Spuch C, Trejo JL, Antequera D, Torres-Aleman I. Choroid plexus megalin is involved in neuroprotection by serum insulin-like growth factor I. J Neurosci. 2005;25:10884-10893.
50. Dietrich MO, Spuch C, Antequera D, Rodal I, de Yebenes JG, Molina JA, Bermejo F, Carro E. Megalin mediates the transport of leptin across the blood-CSF barrier. Neurobiol Aging. 2008;29:902-912.
51. Zlokovic BV, Martel CL, Matsubara E, McComb JG, Zheng G, McCluskey RT, Frangione B, Ghiso J. Glycoprotein 330/megalin: probable role in receptormediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid beta at the blood-brain and blood-cerebrospinal fluid barriers. Proc Natl Acad Sci USA. 1996;93:4229-4234.
52. Rubin EM, Ishida BY, Clift SM, Krauss RM. Expression of human apolipoprotein A-I in transgenic mice results in reduced plasma levels of murine apolipoprotein A-I and the appearance of two new high density lipoprotein size subclasses. Proc Natl Acad Sci USA. 1991;88:434-438.
53. Chiba H, Akita H, Hui SP, Takahashi Y, Nagasaka H, Fuda H, Kobayashi K. Effects of triamcinolone on brain and cerebrospinal fluid apolipoprotein E levels in rats. Life Sci. 1997;60:1757-1761.
54. Saito K, Seishima M, Heyes MP, Song H, Fujigaki S, Maeda S, Vickers JH, Noma A. Marked increases in concentrations of apolipoprotein in the cerebrospinal fluid of poliovirus-infected macaques: relations between apolipoprotein concentrations and severity of brain injury. Biochem J. 1997;321(Pt 1):145-149.
55. Koch S, Donarski N, Goetze K, Kreckel M, Stuerenburg HJ, Buhmann C, Beisiegel U. Characterization of four lipoprotein classes in human cerebrospinal fluid. J Lipid Res. 2001;42:1143-1151.
56. Pitas RE, Boyles JK, Lee SH, Hui D, Weisgraber KH. Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B, E(Ldl) receptors in the brain. J Biol Chem. 1987;262:14352-14360.
57. Johanson CE, Duncan JA III, Klinge PM, Brinker T, Stopa EG, Silverberg GD. Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res. 2008;5:10.
58. Perez-Gracia E, Blanco R, Carmona M, Carro E, Ferrer I. Oxidative stress damage and oxidative stress responses in the choroid plexus in Alzheimer's disease. Acta Neuropathol. 2009;118:497-504.
59. Vargas T, Ugalde C, Spuch C, Antequera D, Moran MJ, Martin MA, Ferrer I, Bermejo-Pareja F, Carro E. Abeta accumulation in choroid plexus is associated with mitochondrial-induced apoptosis. Neurobiol Aging. 2010;31:1569-1581.