Multi-dimensional mass spectrometry-based shotgun lipidomics and the altered lipids at the mild cognitive impairment stage of Alzheimer's disease

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1801, Issue 8, 2010, Pages 774-783

  Han, Xianlin ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Apolipoprotein E; Ceramide; Electrospray ionization mass spectrometry; Plasmalogen; Shotgun lipidomics; Sulfatide

Indexed keywords

APOLIPOPROTEIN E; CERAMIDE; LOW DENSITY LIPOPROTEIN RECEPTOR; PLASMALOGEN; SULFATIDE;

DISEASE COURSE; GEL ELECTROPHORESIS; GENETIC RISK; HUMAN; HYDROPHOBICITY; IONIZATION; LIPID ANALYSIS; LIPIDOMICS; LIPOPROTEIN METABOLISM; MASS SPECTROMETRY; MILD COGNITIVE IMPAIRMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN TRANSPORT; REVIEW;

ALZHEIMER DISEASE; ANIMALS; BRAIN CHEMISTRY; COGNITION; HUMANS; LIPID METABOLISM; LIPIDS; MASS SPECTROMETRY; MODELS, BIOLOGICAL; SULFOGLYCOSPHINGOLIPIDS;

EID: 77953254984     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2010.01.010     Document Type: Review

References (93)

1. Han X., and Gross R.W. Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J. Lipid Res. 44 (2003) 1071-1079
2. Lagarde M., Geloen A., Record M., Vance D., and Spener F. Lipidomics is emerging. Biochim. Biophys. Acta 1634 (2003) 61
3. Pulfer M., and Murphy R.C. Electrospray mass spectrometry of phospholipids. Mass Spectrom. Rev. 22 (2003) 332-364
4. Griffiths W.J. Tandem mass spectrometry in the study of fatty acids, bile acids, and steroids. Mass Spectrom. Rev. 22 (2003) 81-152
5. Byrdwell W.C. APCI-MS lipid analysis. Oily Press Lipid Library 16 (2003) 171-253
6. Han X., and Gross R.W. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of the cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24 (2005) 367-412
7. Hsu F.-F., and Turk J. Electrospray ionization with low-energy collisionally activated dissociation tandem mass spectrometry of complex lipids: structural characterization and mechanism of fragmentation. In: Byrdwell W.C. (Ed). Modern Methods for Lipid Analysis by Liquid Chromatography/Mass Spectrometry and Related Techniques (2005), AOCS Press, Champaign, Ill 61-178
8. Schiller J., Suss R., Fuchs B., Muller M., Zschornig O., and Arnold K. MALDI-TOF MS in lipidomics. Front. Biosci. 12 (2007) 2568-2579
9. Han X., and Gross R.W. Shotgun lipidomics: multi-dimensional mass spectrometric analysis of cellular lipidomes. Expert Rev. Proteomics 2 (2005) 253-264
10. Han X., and Gross R.W. Quantitative analysis and molecular species fingerprinting of triacylglyceride molecular species directly from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal. Biochem. 295 (2001) 88-100
11. Han X., Yang J., Cheng H., Ye H., and Gross R.W. Towards fingerprinting cellular lipidomes directly from biological samples by two-dimensional electrospray ionization mass spectrometry. Anal. Biochem. 330 (2004) 317-331
12. Jiang X., Cheng H., Yang K., Gross R.W., and Han X. Alkaline methanolysis of lipid extracts extends shotgun lipidomics analyses to the low abundance regime of cellular sphingolipids. Anal. Biochem. 371 (2007) 135-145
13. Yang K., Cheng H., Gross R.W., and Han X. Automated lipid identification and quantification by multi-dimensional mass spectrometry-based shotgun lipidomics. Anal. Chem. 81 (2009) 4356-4368
14. Cheng H., Jiang X., and Han X. Alterations in lipid homeostasis of mouse dorsal root ganglia induced by apolipoprotein E deficiency: a shotgun lipidomics study. J. Neurochem. 101 (2007) 57-76
15. Han X., Yang K., and Gross R.W. Microfluidics-based electrospray ionization enhances intrasource separation of lipid classes and extends identification of individual molecular species through multi-dimensional mass spectrometry: development of an automated high throughput platform for shotgun lipidomics. Rapid Commun. Mass Spectrom. 22 (2008) 2115-2124
16. Han X., and Gross R.W. Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 10635-10639
17. Han X., Gubitosi-Klug R.A., Collins B.J., and Gross R.W. Alterations in individual molecular species of human platelet phospholipids during thrombin stimulation: electrospray ionization mass spectrometry-facilitated identification of the boundary conditions for the magnitude and selectivity of thrombin-induced platelet phospholipid hydrolysis. Biochemistry 35 (1996) 5822-5832
18. Han X., Yang K., Yang J., Fikes K.N., Cheng H., and Gross R.W. Factors influencing the electrospray intrasource separation and selective ionization of glycerophospholipids. J. Am. Soc. Mass Spectrom. 17 (2006) 264-274
19. Koivusalo M., Haimi P., Heikinheimo L., Kostiainen R., and Somerharju P. Quantitative determination of phospholipid compositions by ESI-MS: effects of acyl chain length, unsaturation, and lipid concentration on instrument response. J. Lipid Res. 42 (2001) 663-672
20. Kim H.Y., Wang T.C., and Ma Y.C. Liquid chromatography/mass spectrometry of phospholipids using electrospray ionization. Anal. Chem. 66 (1994) 3977-3982
21. Yang K., Zhao Z., Gross R.W., and Han X. Systematic analysis of choline-containing phospholipids using multi-dimensional mass spectrometry-based shotgun lipidomics. J. Chromatogr. B 877 (2009) 2924-2936
22. Han X., Yang K., Yang J., Cheng H., and Gross R.W. Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples. J. Lipid Res. 47 (2006) 864-879
23. Han X., Yang K., Cheng H., Fikes K.N., and Gross R.W. Shotgun lipidomics of phosphoethanolamine-containing lipids in biological samples after one-step in situ derivatization. J. Lipid Res. 46 (2005) 1548-1560
24. Cheng H., Guan S., and Han X. Abundance of triacylglycerols in ganglia and their depletion in diabetic mice: implications for the role of altered triacylglycerols in diabetic neuropathy. J. Neurochem. 97 (2006) 1288-1300
25. Han X., Holtzman D.M., and McKeel Jr. D.W. Plasmalogen deficiency in early Alzheimer's disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J. Neurochem. 77 (2001) 1168-1180
26. Yankner B.A. New clues to Alzheimer's disease: unraveling the roles of amyloid and tau. Nat. Med. 2 (1996) 850-852
27. Morishima-Kawashima M., and Ihara Y. Alzheimer's disease: beta-amyloid protein and tau. J. Neurosci. Res. 70 (2002) 392-401
28. Selkoe D.J. Alzheimer disease: mechanistic understanding predicts novel therapies. Ann. Intern. Med. 140 (2004) 627-638
29. Armstrong R.A., Winsper S.J., and Blair J.A. Aluminium and Alzheimer's disease: review of possible pathogenic mechanisms. Dementia 7 (1996) 1-9
30. Cummings J.L., and Cole G. Alzheimer disease. Jama 287 (2002) 2335-2338
31. McGeer E.G., and McGeer P.L. Inflammatory processes in Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 27 (2003) 741-749
32. Albers D.S., and Beal M.F. Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease. J. Neural Transm. Suppl. 59 (2000) 133-154
33. Mattson M.P. Will caloric restriction and folate protect against AD and PD?. Neurology 60 (2003) 690-695
34. Tabet N. Acetylcholinesterase inhibitors for Alzheimer's disease: anti-inflammatories in acetylcholine clothing!. Age Ageing 35 (2006) 336-338
35. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response?. Nat. Med. 12 (2006) 1005-1015
36. Onyango I.G., and Khan S.M. Oxidative stress, mitochondrial dysfunction, and stress signaling in Alzheimer's disease. Curr. Alz. Res. 3 (2006) 339-349
37. Sivaprakasam K. Towards a unifying hypothesis of Alzheimer's disease: cholinergic system linked to plaques, tangles and neuroinflammation. Curr. Med. Chem. 13 (2006) 2179-2188
38. Hauptmann S., Keil U., Scherping I., Bonert A., Eckert A., and Mueller W.E. Mitochondrial dysfunction in sporadic and genetic Alzheimer's disease. Exp. Gerontol. 41 (2006) 668-673
39. Strittmatter W.J., and Roses A.D. Apolipoprotein E and Alzheimer's disease. Annu. Rev. Neurosci. 19 (1996) 53-77
40. Cedazo-Minguez A., and Cowburn R.F. Apolipoprotein E: a major piece in the Alzheimer's disease puzzle. J. Cell. Mol. Med. 5 (2001) 254-266
41. Holtzman D.M. In vivo effects of ApoE and clusterin on amyloid-beta metabolism and neuropathology. J. Mol. Neurosci. 23 (2004) 247-254
42. Mahley R.W. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240 (1988) 622-630
43. Han X. The role of apolipoprotein E in lipid metabolism in the central nervous system. Cell. Mol. Life Sci. 61 (2004) 1896-1906
44. Han X., Holtzman D.M., McKeel Jr. D.W., Kelley J., and Morris J.C. Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J. Neurochem. 82 (2002) 809-818
45. Guan Z., Wang Y., Cairns N.J., Lantos P.L., Dallner G., and Sindelar P.J. Decrease and structural modifications of phosphatidylethanolamine plasmalogen in the brain with Alzheimer disease. J. Neuropathol. Exp. Neurol. 58 (1999) 740-747
46. Klein J. Membrane breakdown in acute and chronic neurodegeneration: focus on choline-containing phospholipids. J. Neural Transm. 107 (2000) 1027-1063
47. Mulder C., Wahlund L.O., Teerlink T., Blomberg M., Veerhuis R., van Kamp G.J., Scheltens P., and Scheffer P.G. Decreased lysophosphatidylcholine/phosphatidylcholine ratio in cerebrospinal fluid in Alzheimer's disease. J. Neural Transm. 110 (2003) 949-955
48. Pettegrew J.W., Panchalingam K., Hamilton R.L., and McClure R.J. Brain membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 26 (2001) 771-782
49. Morris J.C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43 (1993) 2412-2414
50. Han X. Lipid alterations in the earliest clinically recognizable stage of Alzheimer's disease: implication of the role of lipids in the pathogenesis of Alzheimer's disease. Curr. Alz. Res. 2 (2005) 65-77
51. Han X. Potential mechanisms contributing to sulfatide depletion at the earliest clinically recognizable stages of Alzheimer's disease: a tale of shotgun lipidomics. J. Neurochem. 103 s1 (2007) 171-179
52. Horrocks L.A., and Sharma M. Plasmalogens and O-alkyl glycerophospholipids. In: Hawthorne J.N., and Ansell G.B. (Eds). Phospholipids (1982), Elsevier Biomedical Press, Amsterdam, The Netherlands 51-93
53. Ginsberg L., Rafique S., Xuereb J.H., Rapoport S.I., and Gershfeld N.L. Disease and anatomic specificity of ethanolamine plasmalogen deficiency in Alzheimer's disease brain. Brain Res. 698 (1995) 223-226
54. Ginsberg L., Xuereb J.H., and Gershfeld N.L. Membrane instability, plasmalogen content, and Alzheimer's disease. J. Neurochem. 70 (1998) 2533-2538
55. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., and Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30 (1991) 572-580
56. Svennerholm L., and Gottfries C.G. Membrane lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early-onset form (type I) and demyelination in late-onset form (type II). J. Neurochem. 62 (1994) 1039-1047
57. DeKosky S.T., Scheff S.W., and Styren S.D. Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 5 (1996) 417-421
58. Peters A., Rosene D.L., Moss M.B., Kemper T.L., Abraham C.R., Tigges J., and Albert M.S. Neurobiological bases of age-related cognitive decline in the rhesus monkey. J. Neuropathol. Exp. Neurol. 55 (1996) 861-874
59. Zoeller R.A., Morand O.H., and Raetz C.R. A possible role for plasmalogens in protecting animal cells against photosensitized killing. J. Biol. Chem. 263 (1988) 11590-11596
60. Scherrer L.A., and Gross R.W. Subcellular distribution, molecular dynamics and catabolism of plasmalogens in myocardium. Mol. Cell. Biochem. 88 (1989) 97-105
61. Brosche T., and Platt D. The biological significance of plasmalogens in defense against oxidative damage. Exp. Gerontol. 33 (1998) 363-369
62. Sindelar P.J., Guan Z., Dallner G., and Ernster L. The protective role of plasmalogens in iron-induced lipid peroxidation. Free Radic. Biol. Med. 26 (1999) 318-324
63. Bassett C.N., and Montine T.J. Lipoproteins and lipid peroxidation in Alzheimer's disease. J. Nutr. Health Aging 7 (2003) 24-29
64. Cheng H., Xu J., McKeel Jr. D.W., and Han X. Specificity and potential mechanism of sulfatide deficiency in Alzheimer's disease: an electrospray ionization mass spectrometric study. Cell. Mol. Biol. 49 (2003) 809-818
65. Farooqui A.A., Horrocks L.A., and Farooqui T. Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions, and involvement in neurological disorders. Chem. Phys. Lipids 106 (2000) 1-29
66. Sanchez-Mejia R.O., Newman J.W., Toh S., Yu G.Q., Zhou Y., Halabisky B., Cisse M., Scearce-Levie K., Cheng I.H., Gan L., Palop J.J., Bonventre J.V., and Mucke L. Phospholipase A2 reduction ameliorates cognitive deficits in a mouse model of Alzheimer's disease. Nat. Neurosci. 11 (2008) 1311-1318
67. Mancuso D.J., Kotzbauer P.T., Wozniak D.F., Sims H.F., Jenkins C.M., Guan S., Han X., Yang K., Sun G., Malik I., Conyers S., Green K.G., Schmidt R.E., and Gross R.W. Genetic ablation of calcium-independent phospholipase A2{gamma} leads to alterations in hippocampal cardiolipin content and molecular species distribution, mitochondrial degeneration, autophagy and cognitive dysfunction. J. Biol. Chem. 284 (2009) 35632-35644
68. Farooqui A.A., and Horrocks L.A. Plasmalogen-selective phospholipase A2 and its involvement in Alzheimer's disease. Biochem. Soc. Trans. 26 (1998) 243-246
69. Vos J.P., Lopes-Cardozo M., and Gadella B.M. Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta 1211 (1994) 125-149
70. Marcus J., and Popko B. Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim. Biophys. Acta 1573 (2002) 406-413
71. von Figura K., Gieselmann V., and Jaeken J. Metachromatic leukodystrophy: lysosomal disorders. In: Sachdev H.S., Beaudet A.L., Sly W.S., and Valle D. (Eds). The Metabolic and Molecular Bases of Inherited Diseases (2001), McGraw-Hill, New York 3695-3724
72. Eckhardt M., Hedayati K.K., Pitsch J., Lullmann-Rauch R., Beck H., Fewou S.N., and Gieselmann V. Sulfatide storage in neurons causes hyperexcitability and axonal degeneration in a mouse model of metachromatic leukodystrophy. J. Neurosci. 27 (2007) 9009-9021
73. Marcus J., Honigbaum S., Shroff S., Honke K., Rosenbluth J., and Dupree J.L. Sulfatide is essential for the maintenance of CNS myelin and axon structure. Glia 53 (2006) 372-381
74. Majocha R.E., Jungalwala F.B., Rodenrys A., and Marotta C.A. Monoclonal antibody to embryonic CNS antigen A2B5 provides evidence for the involvement of membrane components at sites of Alzheimer degeneration and detects sulfatides as well as gangliosides. J. Neurochem. 53 (1989) 953-961
75. Cutler R.G., Kelly J., Storie K., Pedersen W.A., Tammara A., Hatanpaa K., Troncoso J.C., and Mattson M.P. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 2070-2075
76. Morishima-Kawashima M., Han X., Tanimura Y., Hamanaka H., Kobayashi M., Sakurai T., Yokoyama M., Wada K., Nukina N., Fujita S.C., and Ihara Y. Effects of human apolipoprotein E isoforms on the amyloid beta-protein concentration and lipid composition in brain low-density membrane domains. J. Neurochem. 101 (2007) 949-958
77. Cheng H., Zhou Y., Holtzman D.M., and Han X. Apolipoprotein E mediates sulfatide depletion in amyloid precursor protein transgenic animal models of Alzheimer's disease. Neurobiol. Aging (2009) 10.1016/j.neurobiolaging.2008.1007.1020
78. Goni F.M., and Alonso A. Sphingomyelinases: enzymology and membrane activity. FEBS Lett. 531 (2002) 38-46
79. Gulbins E., and Kolesnick R. Acid sphingomyelinase-derived ceramide signaling in apoptosis. Subcell. Biochem. 36 (2002) 229-244
80. Ruvolo P.P., Johnson C.R., and Jarvis W.D. Ceramide-driven stress signals in cancer and aging. Adv. Cell Aging Gerontol. 12 (2003) 47-69
81. Lee J.-T., Xu J., Lee J.-M., Ku G., Han X., Yang D.-I., Chen S., and Hsu C.Y. Amyloid-b peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway. J. Cell Biol. 164 (2004) 123-131
82. Price J.L., and Morris J.C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann. Neurol. 45 (1999) 358-368
83. Morris J.C., Storandt M., Miller J.P., McKeel D.W., Price J.L., Rubin E.H., and Berg L. Mild cognitive impairment represents early-stage Alzheimer disease. Arch. Neurol. 58 (2001) 397-405
84. Han X., Cheng H., Fryer J.D., Fagan A.M., and Holtzman D.M. Novel role for apolipoprotein E in the central nervous system: modulation of sulfatide content. J. Biol. Chem. 278 (2003) 8043-8051
85. Han X., Fagan A.M., Cheng H., Morris J.C., Xiong C., and Holtzman D.M. Cerebrospinal fluid sulfatide is decreased in subjects with incipient dementia. Ann. Neurol. 54 2003 (2003) 115-119 [see comment] [erratum appears in Ann Neurol. Nov;54(5):693]
86. Van Uden E., Kang D.E., Koo E.H., and Masliah E. LDL, receptor-related protein (LRP) in Alzheimer's disease: towards a unified theory of pathogenesis. Microsc. Res. Tech. 50 (2000) 268-272
87. Abdulkarim Y., and Hameed Z. Is the LDL receptor involved in cortical amyloid protein clearance?. Neurochem. Res. 31 (2006) 839-847
88. Mulder M., and Terwel D. Possible link between lipid metabolism and cerebral amyloid angiopathy in Alzheimer's disease: a role for high-density lipoproteins?. Haemostasis 28 (1998) 174-194
89. LaFerla F.M., Troncoso J.C., Strickland D.K., Kawas C.H., and Jay G. Neuronal cell death in Alzheimer's disease correlates with apoE uptake and intracellular Abeta stabilization. J. Clin. Invest. 100 (1997) 310-320
90. Laws S.M., Hone E., Taddei K., Harper C., Dean B., McClean C., Masters C., Lautenschlager N., Gandy S.E., and Martins R.N. Variation at the APOE - 491 promoter locus is associated with altered brain levels of apolipoprotein E. Mol. Psychiatry 7 (2002) 886-890
91. Ulery P.G., and Strickland D.K. LRP in Alzheimer's disease: friend or foe?. J. Clin. Invest. 106 (2000) 1077-1079
92. Herz J., and Strickland D.K. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108 (2001) 779-784
93. Christie W.W., and Han X. Lipid Analysis: Isolation, Separation, Identification and Lipidomic Analysis. Fourth ed. (2010), The Oily Press, Bridgwater, England