Extracorporeal apheresis therapy for Alzheimer disease-targeting lipids, stress, and inflammation.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
17
06
2019
accepted:
24
09
2019
revised:
13
09
2019
pubmed:
9
10
2019
medline:
15
12
2020
entrez:
10
10
2019
Statut:
ppublish
Résumé
Current therapeutic approaches to Alzheimer disease (AD) remain disappointing and, hence, there is an urgent need for effective treatments. Here, we provide a perspective review on the emerging role of "metabolic inflammation" and stress as a key factor in the pathogenesis of AD and propose a novel rationale for correction of metabolic inflammation, increase resilience and potentially slow-down or halt the progression of the neurodegenerative process. Based on recent evidence and observations of an early pilot trial, we posit a potential use of extracorporeal apheresis in the prevention and treatment of AD. Apolipoprotein E, lipoprotein(a), oxidized LDL (low density lipoprotein)'s and large LDL particles, as well as other proinflammatory lipids and stress hormones such as cortisol, have been recognized as key factors in amyloid plaque formation and aggravation of AD. Extracorporeal lipoprotein apheresis systems employ well-established, powerful methods to provide an acute, reliable 60-80% reduction in the circulating concentration of these lipid classes and reduce acute cortisol levels. Following a double-membrane extracorporeal apheresis in patients with AD, there was a significant reduction of proinflammatory lipids, circulating cytokines, immune complexes, proinflammatory metals and toxic chaperones in patients with AD. On the basis of the above, we suggest designing clinical trials to assess the promising potential of such "cerebropheresis" treatment in patients with AD and, possibly, other neurodegenerative diseases.
Identifiants
pubmed: 31595035
doi: 10.1038/s41380-019-0542-x
pii: 10.1038/s41380-019-0542-x
doi:
Substances chimiques
Cholesterol, LDL
0
Lipids
0
Lipoproteins, LDL
0
oxidized low density lipoprotein
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
275-282Subventions
Organisme : Medical Research Council
ID : MC_PC_18052
Pays : United Kingdom
Références
Fitz NF, Nam KN, Koldamova R, Lefterov I. Therapeutic targeting of nuclear receptors, LXR and RXR, for Alzheimer’s disease. Br J Pharmacol. 2019;176:3599–3610.
Ng TP, Feng L, Nyunt MS, Feng L, Gao Q, Lim ML, et al. Metabolic syndrome and the risk of mild cognitive impairment and progression to dementia: follow-up of the Singapore Longitudinal Ageing Study Cohort. JAMA Neurol. 2016;73:456–63.
doi: 10.1001/jamaneurol.2015.4899
pubmed: 26926205
pmcid: 26926205
Furman D, Chang J, Lartigue L, Bolen CR, Haddad F, Gaudilliere B, et al. Expression of specific inflammasome gene modules stratifies older individuals into two extreme clinical and immunological states. Nat Med. 2017;23:174–84.
doi: 10.1038/nm.4267
pubmed: 28092664
pmcid: 28092664
de la Monte SM, Tong M, Daiello LA, Ott BR. Early-stage Alzheimer’s disease is associated with simultaneous systemic and central nervous system dysregulation of insulin-linked metabolic pathways. J Alzheimer's Dis. 2019;68:657–68.
doi: 10.3233/JAD-180906
Sharifipour E, Sharifimoghadam S, Hassanzadeh N, Ghasemian MN, Ghoreishi A, Hejazi SA, et al. Altered plasma visfatin levels and insulin resistance in patients with Alzheimer’s disease. Acta Neurol Belg. 2019. [Epub ahead of print].
Schally AV, Salgueiro L. Part III: Experimental studies on antagonists of LH-RH and GH-RH in animal models of Alzheimer’s disease: projections for treatment of other neurological conditions. Peptides. 2015;72:154–63.
doi: 10.1016/j.peptides.2015.03.009
pubmed: 25843023
pmcid: 25843023
Jaszberenyi M, Rick FG, Szalontay L, Block NL, Zarandi M, Cai RZ, et al. Beneficial effects of novel antagonists of GHRH in different models of Alzheimer’s disease. Aging. 2012;4:755–67.
doi: 10.18632/aging.100504
pubmed: 23211425
pmcid: 23211425
Romero MJ, Lucas R, Dou H, Sridhar S, Czikora I, Mosieri EM, et al. Role of growth hormone-releasing hormone in dyslipidemia associated with experimental type 1 diabetes. Proc Natl Acad Sci USA. 2016;113:1895–1900.
doi: 10.1073/pnas.1525520113
pubmed: 26831066
pmcid: 26831066
Femminella GD, Frangou E, Love SB, Busza G, Holmes C, Ritchie C, et al. Evaluating the effects of the novel GLP-1 analogue liraglutide in Alzheimer’s disease: study protocol for a randomised controlled trial (ELAD study). Trials. 2019;20:191.
doi: 10.1186/s13063-019-3259-x
pubmed: 30944040
pmcid: 30944040
Batista AF, Bodart-Santos V, De Felice FG, Ferreira ST. Neuroprotective actions of glucagon-like peptide-1 (GLP-1) analogues in Alzheimer’s and Parkinson’s diseases. CNS Drugs. 2019;33:209–23.
doi: 10.1007/s40263-018-0593-6
pubmed: 30511349
pmcid: 30511349
Van DP, Lacoste B. Impact of metabolic syndrome on neuroinflammation and the blood-brain barrier. Front Neurosci. 2018;12:930.
doi: 10.3389/fnins.2018.00930
Dempsey C, Rubio AA, Bryson KJ, Finucane O, Larkin C, Mills EL, et al. Inhibiting the NLRP3 inflammasome with MCC950 promotes non-phlogistic clearance of amyloid-beta and cognitive function in APP/PS1 mice. Brain Behav Immun. 2017;61:306–16.
doi: 10.1016/j.bbi.2016.12.014
pubmed: 28003153
pmcid: 28003153
Button EB, Boyce GK, Wilkinson A, Stukas S, Hayat A, Fan J, et al. ApoA-I deficiency increases cortical amyloid deposition, cerebral amyloid angiopathy, cortical and hippocampal astrogliosis, and amyloid-associated astrocyte reactivity in APP/PS1 mice. Alzheimer's Res Ther. 2019;11:44.
doi: 10.1186/s13195-019-0497-9
Marais AD. Apolipoprotein E in lipoprotein metabolism, health and cardiovascular disease. Pathology. 2019;51:165–76.
doi: 10.1016/j.pathol.2018.11.002
pubmed: 30598326
pmcid: 30598326
Lee S, Parekh T, King SM, Reed B, Chui HC, Krauss RM, et al. Low-density lipoprotein particle size subfractions and cerebral amyloidosis. J Alzheimer's Dis. 2019;68:983–90.
doi: 10.3233/JAD-181252
Koch CA, Krabbe S, Hehmke B. Statins, metformin, proprotein-convertase-subtilisin-kexin type-9 (PCSK9) inhibitors and sex hormones: Immunomodulatory properties? Rev Endocr Metab Disord. 2018;19:363–95.
doi: 10.1007/s11154-018-9478-8
pubmed: 30673921
pmcid: 30673921
Koch CA, Antonelli A. Immunoendocrinology: when (neuro)endocrinology and immunology meet. Rev Endocr Metab Disord. 2018;19:277–82.
doi: 10.1007/s11154-018-9479-7
pubmed: 30656554
pmcid: 30656554
Mejias-Trueba M, Perez-Moreno MA, Fernandez-Arche MA. Systematic review of the efficacy of statins for the treatment of Alzheimer’s disease. Clin Med. 2018;18:54–61.
doi: 10.7861/clinmedicine.18-1-54
Leung YY, Toledo JB, Nefedov A, Polikar R, Raghavan N, Xie SX, et al. Identifying amyloid pathology-related cerebrospinal fluid biomarkers for Alzheimer’s disease in a multicohort study. Alzheimer's Dement. 2015;1:339–48.
Wilson DP, Jacobson TA, Jones PH, Koschinsky ML, McNeal CJ, Nordestgaard BG, et al. Use of lipoprotein(a) in clinical practice: a biomarker whose time has come. A scientific statement from the National Lipid Association. J Clin Lipidol. 2019;13:374–92.
doi: 10.1016/j.jacl.2019.04.010
pubmed: 31147269
pmcid: 31147269
Solfrizzi V, Panza F, D’Introno A, Colacicco AM, Capurso C, Basile AM, et al. Lipoprotein(a), apolipoprotein E genotype, and risk of Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 2002;72:732–6.
doi: 10.1136/jnnp.72.6.732
pubmed: 12023414
pmcid: 12023414
Mielke MM, Haughey NJ, Han D, An Y, Bandaru VVR, Lyketsos CG, et al. The association between plasma ceramides and sphingomyelins and risk of Alzheimer’s disease differs by sex and APOE in the Baltimore Longitudinal Study of Aging. J Alzheimer's Dis. 2017;60:819–28.
doi: 10.3233/JAD-160925
Chatterjee P, Lim WL, Shui G, Gupta VB, James I, Fagan AM, et al. Plasma phospholipid and sphingolipid alterations in presenilin1 mutation carriers: a pilot study. J Alzheimer's Dis. 2016;50:887–94.
doi: 10.3233/JAD-150948
Panchal M, Gaudin M, Lazar AN, Salvati E, Rivals I, Ayciriex S, et al. Ceramides and sphingomyelinases in senile plaques. Neurobiol Dis. 2014;65:193–201.
doi: 10.1016/j.nbd.2014.01.010
pubmed: 24486621
pmcid: 24486621
Xing Y, Tang Y, Zhao L, Wang Q, Qin W, Zhang JL, et al. Plasma ceramides and neuropsychiatric symptoms of Alzheimer’s disease. J Alzheimer's Dis. 2016;52:1029–35.
doi: 10.3233/JAD-151158
Kim SH, Yang JS, Lee JC, Lee JY, Lee JY, Kim E, et al. Lipidomic alterations in lipoproteins of patients with mild cognitive impairment and Alzheimer’s disease by asymmetrical flow field-flow fractionation and nanoflow ultrahigh performance liquid chromatography-tandem mass spectrometry. J Chromatogr A. 2018;1568:91–100.
doi: 10.1016/j.chroma.2018.07.018
pubmed: 30007793
pmcid: 30007793
Proitsi P, Kim M, Whiley L, Simmons A, Sattlecker M, Velayudhan L, et al. Association of blood lipids with Alzheimer’s disease: a comprehensive lipidomics analysis. Alzheimer's Dement. 2017;13:140–51.
doi: 10.1016/j.jalz.2016.08.003
Yu Q, He Z, Zubkov D, Huang S, Kurochkin I, Yang X, et al. Lipidome alterations in human prefrontal cortex during development, aging, and cognitive disorders. Mol Psychiatry. 2018. [Epub ahead of print].
Lupien SJ, McEwen BS. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Brain Res Rev. 1997;24:1–27.
doi: 10.1016/S0165-0173(97)00004-0
pubmed: 9233540
pmcid: 9233540
Lee BK, Glass TA, Wand GS, McAtee MJ, Bandeen-Roche K, Bolla KI, et al. Apolipoprotein e genotype, cortisol, and cognitive function in community-dwelling older adults. Am J Psychiatry. 2008;165:1456–64.
doi: 10.1176/appi.ajp.2008.07091532
pubmed: 18593777
pmcid: 18593777
Ouanes S, Castelao E, Gebreab S, von GA, Preisig M, Popp J. Life events, salivary cortisol, and cognitive performance in nondemented subjects: a population-based study. Neurobiol Aging. 2017;51:1–8.
doi: 10.1016/j.neurobiolaging.2016.11.014
pubmed: 28012996
pmcid: 28012996
Sang YM, Wang LJ, Mao HX, Lou XY, Zhu YJ. The association of short-term memory and cognitive impairment with ghrelin, leptin, and cortisol levels in non-diabetic and diabetic elderly individuals. Acta Diabetol. 2018;55:531–9.
doi: 10.1007/s00592-018-1111-5
pubmed: 29492658
pmcid: 29492658
Ouanes S, Popp J. High cortisol and the risk of dementia and Alzheimer’s disease: a review of the literature. Front Aging Neurosci. 2019;11:43.
doi: 10.3389/fnagi.2019.00043
pubmed: 30881301
pmcid: 30881301
Popp J, Wolfsgruber S, Heuser I, Peters O, Hull M, Schroder J, et al. Cerebrospinal fluid cortisol and clinical disease progression in MCI and dementia of Alzheimer’s type. Neurobiol Aging. 2015;36:601–7.
doi: 10.1016/j.neurobiolaging.2014.10.031
pubmed: 25435336
pmcid: 25435336
Fitzsimons CP, van Hooijdonk LW, Schouten M, Zalachoras I, Brinks V, Zheng T, et al. Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psychiatry. 2013;18:993–1005.
doi: 10.1038/mp.2012.123
pubmed: 22925833
pmcid: 22925833
Moreno-Jimenez EP, Flor-Garcia M, Terreros-Roncal J, Rabano A, Cafini F, Pallas-Bazarra N, et al. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med. 2019;25:554–60.
doi: 10.1038/s41591-019-0375-9
pubmed: 30911133
pmcid: 30911133
Bornstein SR. Predisposing factors for adrenal insufficiency. N Engl J Med. 2009;360:2328–39.
doi: 10.1056/NEJMra0804635
pubmed: 19474430
pmcid: 19474430
Ehrhart-Bornstein M, Hinson JP, Bornstein SR, Scherbaum WA, Vinson GP. Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev. 1998;19:101–43.
doi: 10.1210/edrv.19.2.0326
pubmed: 9570034
pmcid: 9570034
Steenblock C, Rubin de Celis MF, Delgadillo Silva LF, Pawolski V, Brennand A, Werdermann M, et al. Isolation and characterization of adrenocortical progenitors involved in the adaptation to stress. Proc Natl Acad Sci USA. 2018;115:12997–3002.
doi: 10.1073/pnas.1814072115
pubmed: 30514817
pmcid: 30514817
Bornstein SR, Steenblock C, Chrousos GP, Schally AV, Beuschlein F, Kline G, et al. Stress-inducible-stem cells: a new view on endocrine, metabolic and mental disease? Mol Psychiatry. 2019;24:2–9.
doi: 10.1038/s41380-018-0244-9
pubmed: 30242231
pmcid: 30242231
Schettler VJJ, Neumann CL, Peter C, Zimmermann T, Julius U, Hohenstein B, et al. Lipoprotein apheresis is an optimal therapeutic option to reduce increased Lp(a) levels. Clin Res Cardiol Suppl. 2019;14(Suppl 1):33–38.
doi: 10.1007/s11789-019-00094-4
pubmed: 30838552
pmcid: 30838552
Leebmann J, Roeseler E, Julius U, Heigl F, Spitthoever R, Heutling D, et al. Lipoprotein apheresis in patients with maximally tolerated lipid-lowering therapy, lipoprotein(a)-hyperlipoproteinemia, and progressive cardiovascular disease: prospective observational multicenter study. Circulation. 2013;128:2567–76.
doi: 10.1161/CIRCULATIONAHA.113.002432
pubmed: 24056686
pmcid: 24056686
Khan TZ, Hsu LY, Arai AE, Rhodes S, Pottle A, Wage R, et al. Apheresis as novel treatment for refractory angina with raised lipoprotein(a): a randomized controlled cross-over trial. Eur Heart J. 2017;38:1561–9.
doi: 10.1093/eurheartj/ehx178
pubmed: 28453721
pmcid: 28453721
Straube R, Voit-Bak K, Gor A, Steinmeier T, Chrousos GP, Boehm BO, et al. Lipid profiles in lyme borreliosis: a potential role for apheresis? Horm Metab Res. 2019;51:326–9.
doi: 10.1055/a-0885-7169
pubmed: 31071737
pmcid: 31071737
Morawietz H, Goettsch W, Brux M, Reimann M, Bornstein SR, Julius U, et al. Lipoprotein apheresis of hypercholesterolemic patients mediates vasoprotective gene expression in human endothelial cells. Atheroscler Suppl. 2013;14:107–13.
doi: 10.1016/j.atherosclerosissup.2012.10.013
pubmed: 23357151
pmcid: 23357151
Orsoni A, Saheb S, Levels JH, Dallinga-Thie G, Atassi M, Bittar R, et al. LDL-apheresis depletes apoE-HDL and pre-beta1-HDL in familial hypercholesterolemia: relevance to atheroprotection. J Lipid Res. 2011;52:2304–13.
doi: 10.1194/jlr.P016816
pubmed: 21957200
pmcid: 21957200
Schettler VJ, Muellendorff F, Schettler E, Platzer C, Norkauer S, Julius U, et al. NMR-based lipoprotein analysis for patients with severe hypercholesterolemia undergoing lipoprotein apheresis or PCSK9-inhibitor therapy (NAPALI-Study). Ther Apher Dial. 2019. [Epub ahead of print].
Lappegard KT, Kjellmo CA, Ljunggren S, Cederbrant K, Marcusson-Stahl M, Mathisen M, et al. Lipoprotein apheresis affects lipoprotein particle subclasses more efficiently compared to the PCSK9 inhibitor evolocumab, a pilot study. Transfus Apher Sci. 2018;57:91–96.
doi: 10.1016/j.transci.2018.01.002
pubmed: 29398508
pmcid: 29398508
Kopprasch S, Bornstein SR, Bergmann S, Graessler J, Hohenstein B, Julius U. Long-term follow-up of circulating oxidative stress markers in patients undergoing lipoprotein apheresis by Direct Adsorption of Lipids (DALI). Atheroscler Suppl. 2017;30:115–21.
doi: 10.1016/j.atherosclerosissup.2017.05.029
pubmed: 29096826
pmcid: 29096826
Kopprasch S, Bornstein SR, Bergmann S, Graessler J, Julius U. Long-term therapeutic efficacy of lipoprotein apheresis on circulating oxidative stress parameters—a comparison of two different apheresis techniques. Atheroscler Suppl. 2015;18:80–84.
doi: 10.1016/j.atherosclerosissup.2015.02.016
pubmed: 25936309
pmcid: 25936309
Tselmin S, Schmitz G, Julius U, Bornstein SR, Barthel A, Graessler J. Acute effects of lipid apheresis on human serum lipidome. Atheroscler Suppl. 2009;10:27–33.
doi: 10.1016/S1567-5688(09)71806-9
pubmed: 20129370
pmcid: 20129370
Baglietto-Vargas D, Medeiros R, Martinez-Coria H, LaFerla FM, Green KN. Mifepristone alters amyloid precursor protein processing to preclude amyloid beta and also reduces tau pathology. Biol Psychiatry. 2013;74:357–66.
doi: 10.1016/j.biopsych.2012.12.003
pubmed: 23312564
pmcid: 23312564
Lesuis SL, Weggen S, Baches S, Lucassen PJ, Krugers HJ. Targeting glucocorticoid receptors prevents the effects of early life stress on amyloid pathology and cognitive performance in APP/PS1 mice. Transl Psychiatry. 2018;8:53.
doi: 10.1038/s41398-018-0101-2
pubmed: 29491368
pmcid: 29491368
Webster SP, McBride A, Binnie M, Sooy K, Seckl JR, Andrew R, et al. Selection and early clinical evaluation of the brain-penetrant 11beta-hydroxysteroid dehydrogenase type 1 (11beta-HSD1) inhibitor UE2343 (Xanamem). Br J Pharm. 2017;174:396–408.
doi: 10.1111/bph.13699
Walther R, Julius U, Tselmin S, Schatz U, Bornstein SR, Graessler J. Short- and long-term effects of lipoprotein apheresis on plasma hormones in patients with therapy-resistant dyslipidemia. Atheroscler Suppl. 2019. [Epub ahead of print].
Freeman LC, Ting JP. The pathogenic role of the inflammasome in neurodegenerative diseases. J Neurochem. 2016;136(Suppl 1):29–38.
doi: 10.1111/jnc.13217
pubmed: 26119245
pmcid: 26119245
Guedes JR, Lao T, Cardoso AL, El KJ. Roles of microglial and monocyte chemokines and their receptors in regulating Alzheimer’s disease-associated amyloid-beta and tau pathologies. Front Neurol. 2018;9:549.
doi: 10.3389/fneur.2018.00549
pubmed: 30158892
pmcid: 30158892
Haskins M, Jones TE, Lu Q, Bareiss SK. Early alterations in blood and brain RANTES and MCP-1 expression and the effect of exercise frequency in the 3xTg-AD mouse model of Alzheimer’s disease. Neurosci Lett. 2016;610:165–70.
doi: 10.1016/j.neulet.2015.11.002
pubmed: 26547034
pmcid: 26547034
Cameron B, Landreth GE. Inflammation, microglia, and Alzheimer’s disease. Neurobiol Dis. 2010;37:503–9.
doi: 10.1016/j.nbd.2009.10.006
pubmed: 19833208
pmcid: 19833208
Ravindran D, Ridiandries A, Vanags LZ, Henriquez R, Cartland S, Tan JT, et al. Chemokine binding protein ‘M3’ limits atherosclerosis in apolipoprotein E-/- mice. PLoS ONE. 2017;12:e0173224.
doi: 10.1371/journal.pone.0173224
pubmed: 28282403
pmcid: 28282403
Feng X, Gao X, Jia Y, Zhang H, Xu Y. Atorvastatin decreased circulating RANTES levels in impaired glucose tolerance patients with hypercholesterolemia: an interventional study. Diabetes Ther. 2017;8:309–19.
doi: 10.1007/s13300-017-0227-x
pubmed: 28120261
pmcid: 28120261
Reale M, Kamal MA, Velluto L, Gambi D, Di NM, Greig NH. Relationship between inflammatory mediators, Abeta levels and ApoE genotype in Alzheimer disease. Curr Alzheimer Res. 2012;9:447–57.
doi: 10.2174/156720512800492549
pubmed: 22272623
pmcid: 22272623
Seddighi S, Varma V, Thambisetty M. alpha2-macroglobulin in Alzheimer’s disease: new roles for an old chaperone. Biomark Med. 2018;12:311–4.
doi: 10.2217/bmm-2018-0027
pubmed: 29537301
pmcid: 29537301
Tomljenovic L. Aluminum and Alzheimer’s disease: after a century of controversy, is there a plausible link? J Alzheimer's Dis. 2011;23:567–98.
doi: 10.3233/JAD-2010-101494
Meleleo D, Notarachille G, Mangini V, Arnesano F. Concentration-dependent effects of mercury and lead on Abeta42: possible implications for Alzheimer’s disease. Eur Biophys J. 2019;48:173–87.
doi: 10.1007/s00249-018-1344-9
pubmed: 30603762
pmcid: 30603762
Russ TC, Killin LOJ, Hannah J, Batty GD, Deary IJ, Starr JM. Aluminium and fluoride in drinking water in relation to later dementia risk. Br J Psychiatry. 2019:1–6. [Epub ahead of print].
Mostafalou S, Abdollahi M. The link of organophosphorus pesticides with neurodegenerative and neurodevelopmental diseases based on evidence and mechanisms. Toxicology. 2018;409:44–52.
doi: 10.1016/j.tox.2018.07.014
pubmed: 30053494
pmcid: 30053494
Boada M, Ramos-Fernandez E, Guivernau B, Munoz FJ, Costa M, Ortiz AM, et al. Treatment of Alzheimer disease using combination therapy with plasma exchange and haemapheresis with albumin and intravenous immunoglobulin: rationale and treatment approach of the AMBAR (Alzheimer Management By Albumin Replacement) study. Neurologia. 2016;31:473–81.
doi: 10.1016/j.nrl.2014.02.003
pubmed: 25023458
pmcid: 25023458
Kawaguchi K, Saigusa A, Yamada S, Gotoh T, Nakai S, Hiki Y, et al. Toward the treatment for Alzheimer’s disease: adsorption is primary mechanism of removing amyloid beta protein with hollow-fiber dialyzers of the suitable materials, polysulfone and polymethyl methacrylate. J Artif Organs. 2016;19:149–58.
doi: 10.1007/s10047-015-0878-1
pubmed: 26686230
pmcid: 26686230