The brain lipidomes of subcortical ischemic vascular dementia and mixed dementia

Neurobiology of Aging

Volumn 35, Issue 10, 2014, Pages 2369-2381

  Lam, Sin Man ^a,b   Wang, Yuting ^b   Duan, Xinrui ^b   Wenk, Markus R ^b   Kalaria, Raj N ^c   Chen, Christopher P ^d,e   Lai, Mitchell K P ^d,e   Shui, Guanghou ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

Author keywords

Alzheimer's disease; Lipidomics; Mass spectrometry; Mixed dementia; Phospholipids; Sphingolipids; Subcortical ischemic vascular dementia

Indexed keywords

LIPIDOME; LYSOBISPHOSPHATIDIC ACID; PHOSPHATIDIC ACID; PHOSPHOLIPID; SPHINGOLIPID; SPHINGOLIPID FATTY ACYL CHAIN; SULFATIDE; UNCLASSIFIED DRUG; BIS(MONOACYLGLYCERYL)PHOSPHATE; LYSOPHOSPHOLIPID; MONOACYLGLYCEROL;

ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; DEMENTIA; GRAY MATTER; HUMAN; HUMAN TISSUE; LIPID BRAIN LEVEL; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MIXED DEMENTIA; NEUROPATHOLOGY; PRIORITY JOURNAL; SUBCORTICAL ISCHEMIC VASCULAR DEMENTIA; TEMPORAL CORTEX; WHITE MATTER; AGED; CHRONIC DISEASE; DEMENTIA, VASCULAR; FEMALE; MALE; METABOLISM; PATHOLOGY; TEMPORAL LOBE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BRAIN ISCHEMIA; CHROMATOGRAPHY, LIQUID; CHRONIC DISEASE; DEMENTIA, VASCULAR; FEMALE; GRAY MATTER; HUMANS; LYSOPHOSPHOLIPIDS; MALE; MASS SPECTROMETRY; MONOGLYCERIDES; PHOSPHOLIPIDS; SPHINGOLIPIDS; SULFOGLYCOSPHINGOLIPIDS; TEMPORAL LOBE; WHITE MATTER;

EID: 84903820413     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.02.025     Document Type: Article

References (52)

1. Akiguchi I., Tomimoto H., Wakita H., Kawamoto Y., Matsuo A., Ohnishi K., Watanabe T., Budka H. Topographical and cytopathological lesion analysis of the white matter in Binswanger's disease brains. Acta Neuropathol. 2004, 107:563-570.
2. Ben-David O., Pewzner-Jung Y., Brenner O., Laviad E.L., Kogot-Levin A., Weissberg I., Biton I.E., Pienik R., Wang E., Kelly S., Alroy J., Raas-Rothschild A., Friedman A., Brugger B., Merrill A.H., Futerman A.H. Encephalopathy caused by ablation of very long acyl chain ceramide synthesis may be largely due to reduced galactosylceramide levels. J.Biol. Chem. 2011, 286:30022-30033.
3. Bosio A., Binczek E., Stoffel W. Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:13280-13285.
4. Bowen D.M., Smith C.B., White P., Flack R.H., Carrasco L.H., Gedye J.L., Davison A.N. Chemical pathology of this organic dementias. II. Quantitative estimation of cellular changes in post-mortem brains. Brain 1977, 100:427-453.
5. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
6. Chan R.B., Oliveira T.G., Cortes E.P., Honig L.S., Duff K.E., Small S.A., Wenk M.R., Shui G., Di Paolo G. Comparative lipidomic analysis of mouse and human brain with Alzheimer disease. J.Biol. Chem. 2012, 287:2678-2688.
7. Coetzee T., Dupree J.L., Popko B. Demyelination and altered expression of myelin-associated glycoprotein isoforms in the central nervous system of galactolipid-deficient mice. J.Neurosci. Res. 1998, 54:613-622.
8. de la Torre J.C. Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol. 2004, 3:184-190.
9. de la Torre J.C. The vascular hypothesis of Alzheimer's disease: bench to bedside and beyond. Neurodegener Dis. 2010, 7:116-121.
10. Deramecourt V., Slade J.Y., Oakley A.E., Perry R.H., Ince P.G., Maurage C.A., Kalaria R.N. Staging and natural history of cerebrovascular pathology in dementia. Neurology 2012, 78:1043-1050.
11. Dubois B., Feldman H.H., Jacova C., Cummings J.L., Dekosky S.T., Barberger-Gateau P., Delacourte A., Frisoni G., Fox N.C., Galasko D., Gauthier S., Hampel H., Jicha G.A., Meguro K., O'Brien J., Pasquier F., Robert P., Rossor M., Salloway S., Sarazin M., de Souza L.C., Stern Y., Visser P.J., Scheltens P. Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol. 2010, 9:1118-1127.
12. Enciu A.M., Constantinescu S.N., Popescu L.M., Mureşanu D.F., Popescu B.O. Neurobiology of vascular dementia. J.Aging Res. 2011, 2011:1-11.
13. Esiri M.M., Nagy Z., Smith M.Z., Barnetson L., Smith A.D. Cerebrovascular disease and threshold for dementia in the early stages of Alzheimer's disease. Lancet 1999, 354:919-920.
14. Exalto L., Whitmer R., Kappele L., Biessels G. An update on type 2 diabetes, vascular dementia and Alzheimer's disease. Exp. Gerontol. 2012, 47:858-864.
15. Frisoni G.B., Fox N.C., Jack C.R., Scheltens P., Thompson P.M. The clinical use of structural MRI in Alzheimer disease. Nature reviews. Neurology 2010, 6:67-77.
16. Gemmell E., Bosomworth H., Allan L., Hall R., Khundakar A., Oakley A.E., Deramecourt V., Polvikoski T.M., O'Brien J.T., Kalaria R.N. Hippocampal neuronal atrophy and cognitive function in delayed poststroke and aging-related dementias. Stroke 2012, 43:808-814.
17. Glantz L., Avramovich A., Trembovler V., Gurvitz V., Kohen R., Eidelman L.A., Shohami E. Ischemic preconditioning increases antioxidants in the brain and peripheral organs after cerebral ischemia. Exp. Neurol. 2005, 192:117-124.
18. Hachinski V.C. The decline and resurgence of vascular dementia. CMAJ 1990, 142:107-111.
19. Han X., Holtzman D.M., McKeel D.W. Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J.Neurochem. 2001, 77:1168-1180.
20. Han X. Potential mechanisms contributing to sulfatide depletion at the earliest clinically recognizable stage of Alzheimer's disease: a tale of shotgun lipidomics. J.Neurochem. 2007, 103(Suppl 1):171-179.
21. Han X., Holtzman D.M., McKeel D.W., Kelley J., Morris J.C. Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J.Neurochem. 2002, 82:809-818.
22. Haughey N.J., Bandaru V.V., Bae M., Mattson M.P. Roles for dysfunctional sphingolipid metabolism in Alzheimer's disease neuropathogenesis. Biochim. Biophys. Acta (BBA) - Mol. Cell Biol. Lipids 2010, 1801:878-886.
23. Kalaria R.N., Kenny R.A., Ballard C.G., Perry R., Ince P., Polvikoski T. Towards defining the neuropathological substrates of vascular dementia. J.Neurol. Sci. 2004, 226:75-80.
24. Koivusalo M., Jansen M., Somerharju P., Ikonen E. Endocytic trafficking of sphingomyelin depends on its acyl chain length. Mol. Biol. Cell 2007, 18:5113-5123.
25. Laviad E.L., Albee L., Pankova-Kholmyansky I., Epstein S., Park H., Merrill A.H., Futerman A.H. Characterization of ceramide synthase 2: tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J.Biol. Chem. 2008, 283:5677-5684.
26. Lim W., Lam S., Shui G., Mondal A., Ong D., Duan X., Creegan R., Martins I., Sharman M., Taddei K., Verdile G., Wenk M., Martin R. Effects of high fat high cholesterol diet on brain lipid profiles in APOE e3 and APOE e4 knock-in mice. Neurobiol. Aging. 2013, 34:2217-2224.
27. Matsuzaki K., Kato K., Yanagisawa K. Aβ polymerization through interaction with membrane gangliosides. Biochim. Biophys. Acta (BBA) - Mol. Cell Biol. Lipids 2010, 1801:868-877.
28. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., Berg L. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41:479-486.
29. Moretti A., Gorini A., Villa R.F. Pharmacotherapy and prevention of vascular dementia. CNS Neurol. Disord. Drug Targets 2011, 10:370-390.
30. Nitsch R.M., Blusztajn J.K., Pittas A.G., Slack B.E., Growdon J.H., Wurtman R.J. Evidence for a membrane defect in Alzheimer disease brain. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:1671-1675.
31. O'Brien J.T., Erkinjuntti T., Reisberg B., Roman G., Sawada T., Pantoni L., Bowler J.V., Ballard C., DeCarli C., Gorelick P.B., Rockwood K., Burns A., Gauthier S., DeKosky S.T. Vascular cognitive impairment. Lancet Neurol. 2003, 2:89-98.
32. Oliveira T.G., Chan R.B., Tian H., Laredo M., Shui G., Staniszewski A., Zhang H., Wang L., Kim T.W., Duff K.E., Wenk M.R., Arancio O., Di Paolo G. Phospholipase d2 ablation ameliorates Alzheimer's disease-linked synaptic dysfunction and cognitive deficits. J.Neurosci. 2010, 30:16419-16428.
33. Pantoni L., Garcia J.H., Gutierrez J.A. Cerebral white matter is highly vulnerable to ischemia. Stroke 1996, 27:1641-1646. discussion 1647.
34. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010, 9:689-701.
35. Petrovitch H., Ross G.W., Steinhorn S.C., Abbott R.D., Markesbery W., Davis D., Nelson J., Hardman J., Masaki K., Vogt M.R., Launer L., White L.R. AD lesions and infarcts in demented and non-demented Japanese-American men. Ann. Neurol. 2005, 57:98-103.
36. Pettegrew J.W., Panchalingam K., Hamilton R.L., McClure R.J. Brain membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 2001, 26:771-782.
37. Pluta R., Amek M.U. Brain ischemia and ischemic blood-brain barrier as etiological factors in sporadic Alzheimer's disease. Neuropsychiatr. Dis. Treat. 2008, 4:855-864.
38. Rehncrona S., Westerberg E., Åkesson B., Siesjö B.K. Brain cortical fatty acids and phospholipids during and following complete and severe incomplete ischemia. J.Neurochem. 1982, 38:84-93.
39. Román G.C., Erkinjuntti T., Wallin A., Pantoni L., Chui H.C. Subcortical ischaemic vascular dementia. Lancet Neurol. 2002, 1:426-436.
40. Scheibel A.B., Duong T.H., Jacobs R. Alzheimer's disease as a capillary dementia. Ann. Med. 1989, 21:103-107.
41. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
42. Shui G., Cheong W.F., Jappar I.A., Hoi A., Xue Y., Fernandis A.Z., Tan B.K.H., Wenk M.R. Derivatization-independent cholesterol analysis in crude lipid extracts by liquid chromatography/mass spectrometry: applications to a rabbit model for atherosclerosis. J.Chromatogr. A 2011, 1218:4357-4365.
43. Shui G., Guan X.L., Low C.P., Chua G.H., Goh J.S.Y., Yang H., Wenk M.R. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol. Biosyst. 2010, 6:1008-1017.
44. Shui G., Lam S.M., Stebbins J., Kusunoki J., Duan X., Li B., Cheong W.F., Soon D., Kelly R.P., Wenk M.R. Polar lipid derangements in type 2 diabetes mellitus: potential pathological relevance of fatty acyl heterogeneity in sphingolipids. Metabolomics 2013, 9:786-799.
45. Shui G., Stebbins J.W., Lam B.D., Cheong W.F., Lam S.M., Gregoire F., Kusonoki J., Wenk M.R., Oresic M. Comparative plasma lipidome between human and cynomolgus monkey: are plasma polar lipids good biomarkers for diabetic monkeys?. PloS one 2011, 6:e19731.
46. Simonsen A.H., Hagnelius N.O., Waldemar G., Nilsson T.K., McGuire J. Protein markers for the differential diagnosis of vascular dementia and Alzheimer's disease. Int. J. Proteomics 2012, 2012:824024.
47. Small S.A., Gandy S. Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 2006, 52:15-31.
48. Snowdon D.A., Greiner L.H., Mortimer J.A., Riley K.P., Greiner P.A., Markesbery W.R. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 1997, 277:813-817.
49. Steiger H.J., Hänggi D. Ischaemic preconditioning of the brain, mechanisms and applications. Acta Neurochir (Wien) 2007, 149:1-10.
50. Tomimoto H. Subcortical vascular dementia. Neurosci. Res. 2011, 71:193-199.
51. Wallin A., Gottfries C.G., Karlsson I., Svennerholm L. Decreased myelin lipids in Alzheimer's disease and vascular dementia. Acta Neurol. Scand. 1989, 80:319-323.
52. Yoshida S., Inoh S., Asano T., Sano K., Kubota M., Shimazaki H., Ueta N. Effect of transient ischemia on free fatty acids and phospholipids in the gerbil brain. Lipid peroxidation as a possible cause of postischemic injury. J.Neurosurg. 1980, 53:323-331.