Specific lipid alterations in alzheimer’s disease and diabetes: Shotgun global cellular lipidome analyses by electrospray ionization mass spectrometry using intrasource separation

Functional Lipidomics

Volumn , Issue , 2005, Pages 285-306

  Han, Xianlin ^a   Gross, Richard W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 17244363903     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420027655     Document Type: Chapter

References (87)

1. Friedman, J.M. Obesity in the new millennium. Nature 2000, 404(6778), 632-634.
2. Tuomilehto, J., Lindstrom, J., Eriksson, J.G., Valle, T.T., Hamalainen, H., Ilanne-Parikka, P., Keinanen-Kiukaanniemi, S., Laakso, M., Louheranta, A., Rastas, M., Salminen, V., and Uusitupa, M. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N. Engl. J. Med. 2001, 344(18), 1343-1350.
3. Sinha, R., Fisch, G., Teague, B., Tamborlane, W.V., Banyas, B., Allen, K., Savoye, M., Rieger, V., Taksali, S., Barbetta, G., Sherwin, R.S., and Caprio, S. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N. Engl. J. Med. 2002, 346(11), 802-810.
4. Bhargava, S.K., Sachdev, H.S., Fall, C.H., Osmond, C., Lakshmy, R., Barker, D.J., Biswas, S.K., Ramji, S., Prabhakaran, D., and Reddy, K.S. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. N. Engl. J. Med. 2004, 350(9), 865-875.
5. Kenchaiah, S., Evans, J.C., Levy, D., Wilson, P.W., Benjamin, E.J., Larson, M.G., Kannel, W.B., and Vasan, R.S. Obesity and the risk of heart failure. N. Engl. J. Med. 2002, 347(5), 305-313.
6. Chauhan, N.B. Membrane dynamics, cholesterol homeostasis, and Alzheimer’s disease. J. Lipid Res. 2003, 44(11), 2019-2029.
7. Koudinov, A.R. and Koudinova, N.V. Cholesterol, synaptic function and Alzheimer’s disease. Pharmacopsychiatry 2003, 36 Suppl. 2, S107-112.
8. McLaurin, J., Darabie, A.A., and Morrison, M.R. Cholesterol, a modulator of membrane-associated Abeta-fibrillogenesis. Pharmacopsychiatry 2003, 36 Suppl. 2, S130-135.
9. Poirier, J. Apolipoprotein E and cholesterol metabolism in the pathogenesis and treatment of Alzheimer’s disease. Trends Mol. Med. 2003, 9(3), 94-101.
10. Puglielli, L., Tanzi, R.E., and Kovacs, D.M. Alzheimer’s disease: the cholesterol connection. Nat. Neurosci. 2003, 6(4), 345-351.
11. Yanagisawa, K. Cholesterol and Abeta aggregation. Pharmacopsychiatry 2003, 36 Suppl. 2, S127-129.
12. Miller, L.J. and Chacko, R. The role of cholesterol and statins in Alzheimer’s disease. Ann. Pharmacother. 2004, 38(1), 91-98.
13. Wolozin, B. Cholesterol and the biology of Alzheimer’s disease. Neuron 2004, 41(1), 7-10.
14. Han, X. Lipid alterations in the earliest clinical stage of Alzheimer’s disease: Implication of the role of lipids in the pathogenesis of Alzheimer’s disease. Curr. Alz. Res. 2004, 1, 2005, 2, 65-77.
15. Holtzman, D.M. Abeta conformational change is central to Alzheimer’s disease. Neurobiol. Aging 2002, 23(6), 1085-1088.
16. Strittmatter, W.J. and Roses, A.D. Apolipoprotein E and Alzheimer’s disease. Annu. Rev. Neurosci. 1996, 19, 53-77.
17. Cedazo-Minguez, A. and Cowburn, R.F. Apolipoprotein E: a major piece in the Alzheimer’s disease puzzle. J. Cell. Mol. Med. 2001, 5(3), 254-266.
18. Bales, K.R., Dodart, J.C., DeMattos, R.B., Holtzman, D.M., and Paul, S.M. Apolipoprotein E, amyloid, and Alzheimer disease. Mol. Interv. 2002, 2(6), 363-375, 339.
19. Raffai, R.L. and Weisgraber, K.H. Cholesterol: from heart attacks to Alzheimer’s disease. J. Lipid Res. 2003, 44(8), 1423-1430.
20. Mahley, R.W. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240(4852), 622-630.
21. Han, X. The role of apolipoprotein E in lipid metabolism in the central nervous system. Cell. Mol. Life Sci. 2004, 61(15), 1896-1906.
22. Gross, R.W. High plasmalogen and arachidonic acid content of canine myocardial sarcolemma: a fast atom bombardment mass spectroscopic and gas chromatographymass spectroscopic characterization. Biochemistry 1984, 23(1), 158-165.
23. Gross, R.W. Identification of plasmalogen as the major phospholipid constituent of cardiac sarcoplasmic reticulum. Biochemistry 1985, 24(7), 1662-1668.
24. Pak, J.H., Bork, V.P., Norberg, R.E., Creer, M.H., Wolf, R.A., and Gross, R.W. Disparate molecular dynamics of plasmenylcholine and phosphatidylcholine bilayers. Biochemistry 1987, 26(15), 4824-4830.
25. Ford, D.A. and Gross, R.W. Identification of endogenous 1-O-alk-1-enyl-2-acyl-snglycerol in myocardium and its effective utilization by choline phosphotransferase. J. Biol. Chem. 1988, 263(6), 2644-2650.
26. Ford, D.A. and Gross, R.W. Plasmenylethanolamine is the major storage depot for arachidonic acid in rabbit vascular smooth muscle and is rapidly hydrolyzed after angiotensin II stimulation. Proc. Natl. Acad. Sci. U. S. A. 1989, 86(10), 3479-3483.
27. Ford, D.A. and Gross, R.W. Differential metabolism of diradyl glycerol molecular subclasses and molecular species by rabbit brain diglyceride kinase. J. Biol. Chem. 1990, 265(21), 12280-12286.
28. Han, X. and Gross, R.W. Plasmenylcholine and phosphatidylcholine membrane bilayers possess distinct conformational motifs. Biochemistry 1990, 29(20), 4992-4996.
29. Hazen, S.L., Stuppy, R.J. and Gross, R.W. Purification and characterization of canine myocardial cytosolic phospholipase A2. A calcium-independent phospholipase with absolute sn-2 regiospecificity for diradyl glycerophospholipids. J. Biol. Chem. 1990, 265(18), 10622-10630.
30. Han, X., Chen, X., and Gross, R.W. Chemical and magnetic inequivalence of glycerol protons in individual subclasses of choline glycerophospholipids: implications for subclass-specific changes in membrane conformational states. J. Am. Chem. Soc. 1991, 113(19), 7104-7109.
31. Creer, M.H. and Gross, R.W. Separation of isomeric lysophospholipids by reverse phase HPLC. Lipids 1985, 20(12), 922-928.
32. Gross, R.W. and Sobel, B.E. Isocratic high-performance liquid chromatography separation of phosphoglycerides and lysophosphoglycerides. J. Chromatogr. 1980, 197(1), 79-85.
33. Taguchi, R., Hayakawa, J., Takeuchi, Y., and Ishida, M. Two-dimensional analysis of phospholipids by capillary liquid chromatography/electrospray ionization mass spectrometry. J. Mass Spectrom. 2000, 35(8), 953-966.
34. DeLong, C.J., Baker, P.R.S., Samuel, M., Cui, Z., andThomas, M.J. Molecular species composition of rat liver phospholipids by ESI-MS/MS: the effect of chromatography. J. Lipid Res. 2001, 42(12), 1959-1968.
35. Koivusalo, M., Haimi, P., Heikinheimo, L., Kostiainen, R., 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. 2001, 42(4), 663-672.
36. 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. 2003, 44(6), 1071-1079.
37. 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. 2005, 24, 367-412.
38. Fenn, J.B., Mann, M., Meng, C.K., Wong, S.F., and Whitehouse, C.M. Electrospray ionization for mass spectrometry of large biomolecules. Science 1989, 246(4926), 64-71.
39. Han, X. and Gross, R.W. Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(22), 10635-10639.
40. Duffin, K.L., Henion, J.D., and Shieh, J.J. Electrospray and tandem mass spectrometric characterization of acylglycerol mixtures that are dissolved in nonpolar solvents. Anal. Chem. 1991, 63(17), 1781-1788.
41. Weintraub, S.T., Pinckard, R.N., and Hail, M. Electrospray ionization for analysis of platelet-activating factor. Rapid Commun. Mass Spectrom. 1991, 5(7), 309-311.
42. Kerwin, J.L., Tuininga, A.R., and Ericsson, L.H. Identification of molecular species of glycerophospholipids and sphingomyelin using electrospray mass spectrometry. J. Lipid Res. 1994, 35(6), 1102-1114.
43. Kim, H.Y., Wang, T.C., and Ma, Y.C. Liquid chromatography/mass spectrometry of phospholipids using electrospray ionization. Anal. Chem. 1994, 66(22), 3977-3982.
44. 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 1996, 35(18), 5822-5832.
45. Lehmann, W.D., Koester, M., Erben, G., and Keppler, D. Characterization and quantification of rat bile phosphatidylcholine by electrospray-tandem mass spectrometry. Anal. Biochem. 1997, 246(1), 102-110.
46. Schneiter, R., Brugger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G., Paltauf, F., Wieland, F.T., and Kohlwein, S.D. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell Biol. 1999, 146(4), 741-754.
47. Brugger, B., Sandhoff, R., Wegehingel, S., Gorgas, K., Malsam, J., Helms, J.B., Lehmann, W.D., Nickel, W., Wieland, F.T. Evidence for segregation of sphingomyelin and cholesterol during formation of COPI-coated vesicles. J. Cell Biol. 2000, 151(3), 507-518.
48. Blom, T.S., Koivusalo, M., Kuismanen, E., Kostiainen, R., Somerharju, P., and Ikonen, E. Mass Spectrometric Analysis Reveals an Increase in Plasma Membrane Polyunsaturated Phospholipid Species upon Cellular Cholesterol Loading. Biochemistry 2001, 40(48), 14635-14644.
49. Duffin, K.L., Obukowicz, M.G., Salsgiver, W.J., Welsch, D.J., Shieh, C., Raz, A., and Needleman, P. Lipid remodeling in mouse liver and plasma resulting from delta6 fatty acid desaturase inhibition. Lipids 2001, 36(11), 1203-1208.
50. Han, X., Holtzman, D.M., and McKeel, D.W., Jr. Plasmalogen deficiency in early Alzheimer’s disease subjects and in animal models: molecular characterization using electrospray ionization mass spectrometry. J. Neurochem. 2001, 77(4), 1168-1180.
51. Williams, S.D., Hsu, F.F., and Ford, D.A. Electrospray ionization mass spectrometry analyses of nuclear membrane phospholipid loss after reperfusion of ischemic myocardium. J. Lipid Res. 2000, 41(10), 1585-1595.
52. Ekroos, K., Chernushevich, I.V., Simons, K., and Shevchenko, A. Quantitative profiling of phospholipids by multiple precursor ion scanning on a hybrid quadrupole time-of-flight mass spectrometer. Anal. Chem. 2002, 74(5), 941-949.
53. Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H.-E., Rajashekar, C.B., Williams, T.D., and Wang, X. Profiling membrane lipids in plant stress responses. Role of phospholipase Da in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 2002, 277(35), 31994-32002.
54. Esch, S.W., Williams, T.D., Biswas, S., Chakrabarty, A., and Levine, S.M. Sphingolipid profile in the CNS of the twitcher (globoid cell leukodystrophy) mouse: A lipidomics approach. Cell. Mol. Biol. 2003, 49(5), 779-787.
55. Fenn, J.B. Electrospray wings for molecular elephants (Nobel lecture). Angew. Chem. Int. Ed. Engl. 2003, 42(33), 3871-3894.
56. Tanaka, K. The origin of macromolecule ionization by laser irradiation (Nobel lecture). Angew. Chem. Int. Ed. Engl. 2003, 42(33), 3860-3870.
57. Han, X. Characterization and direct quantitation of ceramide molecular species from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal. Biochem. 2002, 302(2), 199-212.
58. Ford, D.A., Han, X., Horner, C.C., and Gross, R.W. Accumulation of unsaturated acylcarnitine molecular species during acute myocardial ischemia: metabolic compartmentalization of products of fatty acyl chain elongation in the acylcarnitine pool. Biochemistry 1996, 35(24), 7903-7909.
59. Kalderon, B., Sheena, V., Shachrur, S., Hertz, R., and Bar-Tana, J. Modulation by nutrients and drugs of liver acyl-CoAs analyzed by mass spectrometry. J. Lipid Res. 2002, 43(7), 1125-1132.
60. 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. 2004, 330(2), 317-331.
61. 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. 2001, 295(1), 88-100.
62. Duffin, K., Obukowicz, M., Raz, A., and Shieh, J.J. Electrospray/tandem mass spectrometry for quantitative analysis of lipid remodeling in essential fatty acid deficient mice. Anal. Biochem. 2000, 279(2), 179-188.
63. Vos, J.P., Lopes-Cardozo, M., and Gadella, B.M. Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta 1994, 1211(2), 125-149.
64. Ishizuka, I. Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res. 1997, 36(4), 245-319.
65. Ikami, T., Ishida, H., and Kiso, M. Synthesis and biological activity of glycolipids, with a focus on gangliosides and sulfatide analogs. Methods Enzymol. 2000, 311, 547-568.
66. Marcus, J. and Popko, B. Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim. Biophys. Acta 2002, 1573(3), 406-413.
67. von Figura, K.; Gieselmann, V.; Jaeken, J. Metachromatic leukodystrophy: Lysosomal disorders. in The Metabolic and Molecular Bases of Inherited Diseases, 8th ed., Sachdev, H.S., Beaudet, A.L., Sly, W.S., Valle, D., Eds., McGraw-Hill: New York, 2001; 3695-3724.
68. Bosio, A., Binczek, E., and 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(23), 13280-13285.
69. Coetzee, T., Fujita, N., Dupree, J., Shi, R., Blight, A., Suzuki, K., and Popko, B. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 1996, 86(2), 209-219.
70. Bosio, A., Bussow, H., Adam, J., and Stoffel, W. Galactosphingolipids and axonoglial interaction in myelin of the central nervous system. Cell Tissue Res. 1998, 292(2), 199-210.
71. Coetzee, T., Dupree, J.L., and Popko, B. Demyelination and altered expression of myelin-associated glycoprotein isoforms in the central nervous system of galactolipiddeficient mice. J. Neurosci. Res. 1998, 54(5), 613-622.
72. Han, X., Holtzman, D.M., McKeel, D.W., Jr., 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. 2002, 82(4), 809-818.
73. Morris, J.C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993, 43(11), 2412-2414.
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. 1989, 53(3), 953-961.
75. 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. 1994, 62(3), 1039-1047.
76. Gottfries, C.G., Karlsson, I., and Svennerholm, L. Membrane components separate early-onset Alzheimer’s disease from senile dementia of the Alzheimer type. Int. Psychogeriatr. 1996, 8(3), 365-372.
77. Cheng, H., Xu, J., McKeel, D.W., Jr., and Han, X. Specificity and potential mechanism of sulfatide deficiency in Alzheimer’s disease: An electrospray ionization mass spectrometric study. Cell. Mol. Biol. 2003, 49(5), 809-818.
78. 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. 2003, 54(1), 115-119.
79. 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. 2003, 278(10), 8043-8051.
80. 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. 2000, 50(4), 268-272.
81. 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 1998, 28(3-4), 174-194.
82. Irizarry, M.C. A turn of the sulfatide in Alzheimer’s disease. Ann. Neurol. 2003, 54(1), 7-8.
83. Hazen, S.L., Hall, C.R., Ford, D.A., and Gross, R.W. Isolation of a human myocardial cytosolic phospholipase A2 isoform. Fast atom bombardment mass spectroscopic and reverse-phase high pressure liquid chromatography identification of choline and ethanolamine glycerophospholipid substrates. J. Clin. Invest. 1993, 91(6), 2513-2522.
84. Han, X., Abendschein, D.R., Kelley, J.G., and Gross, R.W. Diabetes-induced changes in specific lipid molecular species in rat myocardium. Biochem. J. 2000, 352(1), 79-89.
85. Finck, B.N., Lehman, J.J., Leone, T.C., Welch, M.J., Bennett, M.J., Kovacs, A., Han, X., Gross, R.W., Kozak, R., Lopaschuk, G.D., and Kelly, D.P. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J. Clin. Invest. 2002, 109(1), 121-130.
86. Finck, B.N., Han, X., Courtois, M., Aimond, F., Nerbonne, J.M., Kovacs, A., Gross, R.W., and Kelly, D.P. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(3), 1226-1231.
87. Bligh, E.G. and Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911-917.