The pathogenic implication of abnormal interaction between apolipoprotein e isoforms, amyloid-beta peptides, and sulfatides in alzheimer's disease

Molecular Neurobiology

Volumn 41, Issue 2-3, 2010, Pages 97-106

  Han, Xianlin ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid beta peptides; Apolipoprotein E; Electrospray ionization mass spectrometry; Lipidomics; Shotgun lipidomics; Sulfatides

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; APOLIPOPROTEIN E4; SULFATIDE; ISOPROTEIN; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; BINDING AFFINITY; CEREBROSPINAL FLUID; CONFERENCE PAPER; DISEASE COURSE; GENETIC ASSOCIATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RISK FACTOR; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; TRANSGENIC ANIMAL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOLIPOPROTEINS E; HUMANS; MOLECULAR STRUCTURE; PEPTIDE FRAGMENTS; PROTEIN ISOFORMS; SULFOGLYCOSPHINGOLIPIDS;

EID: 77955088921     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-009-8092-x     Document Type: Conference Paper

References (84)

1. Yankner BA (1996) New clues to Alzheimer's disease: unraveling the roles of amyloid and tau. Nat Med 2:850-852
2. Selkoe DJ (1997) Alzheimer's disease: genotypes, phenotypes, and treatments. Science 275:630-631
3. Holtzman DM (2002) Abeta conformational change is central to Alzheimer's disease. Neurobiol Aging 23:1085-1088
4. Morishima-Kawashima M, Ihara Y (2002) Alzheimer's disease: beta-amyloid protein and tau. J Neurosci Res 70:392-401
5. McGeer EG, McGeer PL (2003) Inflammatory processes in Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 27:741-749
6. Selkoe DJ (2006) The ups and downs of Abeta. Nat Med 12:758-759, discussion 759
7. Wisniewski KE, Wisniewski HM, Wen GY (1985) Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome. Ann Neurol 17:278-282
8. Fan J, Donkin J, Wellington C (2009) Greasing the wheels of Abeta clearance in Alzheimer's disease: the role of lipids and apolipoprotein E. Biofactors 35:239-248
9. Fagan AM, Head D, Shah AR, Marcus D, Mintun M, Morris JC, Holtzman DM (2009) Decreased cerebrospinal fluid Abeta(42) correlates with brain atrophy in cognitively normal elderly. Ann Neurol 65:176-183
10. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE (2009) Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29:4252-4262
11. Zerbinatti CV, Wahrle SE, Kim H, Cam JA, Bales K, Paul SM, Holtzman DM, Bu G (2006) Apolipoprotein E and low density lipoprotein receptor-related protein facilitate intraneuronal Abeta42 accumulation in amyloid model mice. J Biol Chem 281:36180-36186
12. Nixon RA (2005) Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases. Neuro-biol Aging 26:373-382
13. Knauer MF, Soreghan B, Burdick D, Kosmoski J, Glabe CG (1992) Intracellular accumulation and resistance to degradation of the Alzheimer amyloid A4/beta protein. Proc Natl Acad Sci USA 89:7437-7441
14. Burdick D, Kosmoski J, Knauer MF, Glabe CG (1997) Preferential adsorption, internalization and resistance to degradation of the major isoform of the Alzheimer's amyloid peptide, A beta 1-42, in differentiated PC12 cells. Brain Res 746:275-284
15. Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622-630
16. DeMattos RB, Brendza RP, Heuser JE, Kierson M, Cirrito JR, Fryer J, Sullivan PM, Fagan AM, Han X, Holtzman DM (2001) Purification and characterization of astrocyte-secreted apolipopro-tein E and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem Int 39:415-425
17. Plump AS, Breslow JL (1995) Apolipoprotein E and the apolipoprotein E-deficient mouse. Annu Rev Nutr 15:495-518
18. Shobab LA, Hsiung G-YR, Feldman HH (2005) Cholesterol in Alzheimer's disease. Lancet Neurology 4:841-852
19. Grimm MO, Grimm HS, Tomic I, Beyreuther K, Hartmann T, Bergmann C (2008) Independent inhibition of Alzheimer disease beta-and gamma-secretase cleavage by lowered cholesterol levels. J Biol Chem 283:11302-11311
20. Curtiss LK, Edgington TS (1978) Identification of a lymphocyte surface receptor for low density lipoprotein inhibitor, an immu-noregulatory species of normal human serum low density lipoprotein. J Clin Invest 61:1298-1308
21. Wisniewski T, Frangione B (1992) Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci Lett 135:235-238
22. Elshourbagy NA, Liao WS, Mahley RW, Taylor JM (1985) Apolipoprotein E mRNA is abundant in the brain and adrenals, as well as in the liver, and is present in other peripheral tissues of rats and marmosets. Proc Natl Acad Sci USA 82:203-207
23. Pitas RE, Boyles JK, Lee SH, Foss D, Mahley RW (1987) Astrocytes synthesize apolipoprotein E and metabolize apolipo-protein E-containing lipoproteins. Biochim Biophys Acta 917:148-161
24. Strittmatter WJ, Roses AD (1996) Apolipoprotein E and Alzheimer's disease. Annu Rev Neurosci 19:53-77
25. Vos JP, Lopes-Cardozo M, Gadella BM (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim Biophys Acta 1211:125-149
26. Ishizuka I (1997) Chemistry and functional distribution of sulfoglycolipids. Prog Lipid Res 36:245-319
27. Ikami T, Ishida H, Kiso M (2000) Synthesis and biological activity of glycolipids, with a focus on gangliosides and sulfatide analogs. Methods Enzymol 311:547-568
28. Marcus J, Popko B (2002) Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim Biophys Acta 1573:406-413
29. Eckhardt M, Hedayati KK, Pitsch J, Lullmann-Rauch R, Beck H, Fewou SN, Gieselmann V (2007) Sulfatide storage in neurons causes hyperexcitability and axonal degeneration in a mouse model of metachromatic leukodystrophy. J Neurosci 27:9009-9021
30. Isaac G, Pernber Z, Gieselmann V, Hansson E, Bergquist J, Mansson JE (2006) Sulfatide with short fatty acid dominates in astrocytes and neurons. Febs J 273:1782-1790
31. Von Figura K, Gieselmann V, Jaeken J (2001) Metachromatic leukodystrophy: lysosomal disorders. In: Sachdev HS, Beaudet AL, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited diseases. McGraw-Hill, New York, pp 3695-3724
32. Molander-Melin M, Pernber Z, Franken S, Gieselmann V, Mansson JE, Fredman P (2004) Accumulation of sulfatide in neuronal and glial cells of arylsulfatase A deficient mice. J Neurocytol 33:417-427
33. Bosio A, Binczek E, Stoffel W (1996) Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc Natl Acad Sci USA 93:13280-13285
34. Coetzee T, Fujita N, Dupree J, Shi R, Blight A, Suzuki K, Popko B (1996) Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 86:209-219
35. Coetzee T, Dupree JL, Popko B (1998) Demyelination and altered expression of myelin-associated glycoprotein isoforms in the central nervous system of galactolipid-deficient mice. J Neurosci Res 54:613-622
36. Bosio A, Bussow H, Adam J, Stoffel W (1998) Galactosphingo-lipids and axono-glial interaction in myelin of the central nervous system. Cell Tissue Res 292:199-210
37. Marcus J, Honigbaum S, Shroff S, Honke K, Rosenbluth J, Dupree JL (2006) Sulfatide is essential for the maintenance of CNS myelin and axon structure. Glia 53:372-381
38. Hu R, Li G, Kamijo Y, Aoyama T, Nakajima T, Inoue T, Node K, Kannagi R, Kyogashima M, Hara A (2007) Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj J 24:565-571
39. Morichika H, Hamanaka Y, Tai T, Ishizuka I (1996) Sulfatides as a predictive factor of lymph node metastasis in patients with colorectal adenocarcinoma. Cancer 78:43-47
40. Svennerholm L, Gottfries CG (1994) 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 62:1039-1047
41. Han X, Holtzman DM, McKeel DW Jr, Kelley J, Morris JC (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease patho-genesis. J Neurochem 82:809-818
42. Cheng H, Xu J, McKeel DW Jr, Han X (2003) Specificity and potential mechanism of sulfatide deficiency in Alzheimer's disease: an electrospray ionization mass spectrometric study. Cell Mol Biol 49:809-818
43. Han X (2007) Potential mechanisms contributing to sulfatide depletion at the earliest clinically recognizable stages of Alzheimer's disease: a tale of shotgun lipidomics. J Neurochem 103 (1):171-179
44. Bognar SK, Furac I, Kubat M, Cosovic C, Demarin V (2002) Croatian population data for arylsulfatase a pseudodeficiency-associated mutations in healthy subjects, and in patients with Alzheimer-type dementia and Down syndrome. Arch Med Res 33:473-477
45. Han X, Gross RW (2003) Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J Lipid Res 44:1071-1079
46. Han X, Gross RW (2005) Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of the cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom Rev 24:367-412
47. Han X, Gross RW (2005) Shotgun lipidomics: multi-dimensional mass spectrometric analysis of cellular lipidomes. Expert Rev Proteomics 2:253-264
48. Han X (2007) Neurolipidomics: challenges and developments. Front Biosci 12:2601-2615
49. Yang K, Cheng H, Gross RW, Han X (2009) Automated lipid identification and quantification by multi-dimensional mass spectrometry-based shotgun lipidomics. Anal Chem 81:4356-4368
50. Han X, Fagan AM, Cheng H, Morris JC, Xiong C, Holtzman DM (2003) Cerebrospinal fluid sulfatide is decreased in subjects with incipient dementia. Ann Neurol 54:115-119
51. Irizarry MC (2003) A turn of the sulfatide in Alzheimer's disease. Ann Neurol 54:7-8
52. Han X, Cheng H, Fryer JD, Fagan AM, Holtzman DM (2003) Novel role for apolipoprotein E in the central nervous system: modulation of sulfatide content. J Biol Chem 278:8043-8051
53. Cheng H, Jiang X, Han X (2007) Alterations in lipid homeostasis of mouse dorsal root ganglia induced by apolipoprotein E deficiency: a shotgun lipidomics study. J Neurochem 101:57-76
54. Cheng H, Zhou Y, Holtzman DM, Han X (2009) Apolipoprotein E mediates sulfatide depletion in amyloid precursor protein trans-genic animal models of Alzheimer's disease. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2008.1007. 1020
55. Van Uden E, Kang DE, Koo EH, Masliah E (2000) LDL receptor-related protein (LRP) in Alzheimer's disease: towards a unified theory of pathogenesis. Microsc Res Tech 50:268-272
56. Arelin K, Kinoshita A, Whelan CM, Irizarry MC, Rebeck GW, Strickland DK, Hyman BT (2002) LRP and senile plaques in Alzheimer's disease: colocalization with apolipoprotein E and with activated astrocytes. Brain Res Mol Brain Res 104:38-46
57. Zeng Y, Cheng H, Jiang X, Han X (2008) Endosomes and lysosomes play distinct roles in sulfatide-induced neuroblastoma apoptosis: potential mechanisms contributing to abnormal sulfatide metabolism in related neuronal diseases. Biochem J 410:81-92
58. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981
59. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE (1994) Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 269:23403-23406
60. Bales KR, Verina T, Dodel RC, Du Y, Altstiel L, Bender M, Hyslop P, Johnstone EM, Little SP, Cummins DJ, Piccardo P, Ghetti B, Paul SM (1997) Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. Nat Genet 17:263-264
61. Holtzman DM, Bales KR, Tenkova T, Fagan AM, Parsadanian M, Sartorius LJ, Mackey B, Olney J, McKeel D, Wozniak D, Paul SM (2000) Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 97:2892-2897
62. Deane R, Wu Z, Sagare A, Davis J, Du Yan S, Hamm K, Xu F, Parisi M, LaRue B, Hu HW, Spijkers P, Guo H, Song X, Lenting PJ, Van Nostrand WE, Zlokovic BV (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43:333-344
63. Holtzman DM, Fagan AM, Mackey B, Tenkova T, Sartorius L, Paul SM, Bales K, Ashe KH, Irizarry MC, Hyman BT (2000) Apolipo-protein E facilitates neuritic and cerebrovascular plaque formation in an Alzheimer's disease model. Ann Neurol 47:739-747
64. Fagan AM, Watson M, Parsadanian M, Bales KR, Paul SM, Holtzman DM (2002) Human and murine ApoE markedly alters A beta metabolism before and after plaque formation in a mouse model of Alzheimer's disease. Neurobiol Dis 9:305-318
65. Fraser PE, Nguyen JT, Chin DT, Kirschner DA (1992) Effects of sulfate ions on Alzheimer beta/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions. J Neurochem 59:1531-1540
66. Castillo GM, Lukito W, Wight TN, Snow AD (1999) The sulfate moieties of glycosaminoglycans are critical for the enhancement of beta-amyloid protein fibril formation. J Neurochem 72:1681-1687
67. Snow AD, Mar H, Nochlin D, Sekiguchi RT, Kimata K, Koike Y, Wight TN (1990) Early accumulation of heparan sulfate in neurons and in the beta-amyloid protein-containing lesions of Alzheimer's disease and Down's syndrome. Am J Pathol 137:1253-1270
68. van Horssen J, Wilhelmus MM, Heljasvaara R, Pihlajaniemi T, Wesseling P, de Waal RM, Verbeek MM (2002) Collagen XVIII: a novel heparan sulfate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer's disease brains. Brain Pathol 12:456-462
69. Zeng Y, Han X (2008) Sulfatides facilitate apolipoprotein E-mediated amyloid-b peptide clearance through an endocytotic pathway. J Neurochem 106:1275-1286
70. Murphy MP, Das P, Nyborg AC, Rochette MJ, Dodson MW, Loosbrock NM, Souder TM, McLendon C, Merit SL, Piper SC, Jansen KR, Golde TE (2003) Overexpression of nicastrin increases Abeta production. FASEB J 17:1138-1140
71. Fagan AM, Younkin LH, Morris JC, Fryer JD, Cole TG, Younkin SG, Holtzman DM (2000) Differences in the Abeta40/Abeta42 ratio associated with cerebrospinal fluid lipoproteins as a function of apolipoprotein E genotype. Ann Neurol 48:201-210
72. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Soriano P, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373:523-527
73. Irizarry MC, Soriano F, McNamara M, Page KJ, Schenk D, Games D, Hyman BT (1997) Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J Neurosci 17:7053-7059
74. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102
75. Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT (1997) APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 56:965-973
76. Kokjohn TA, Roher AE (2009) Amyloid precursor protein transgenic mouse models and Alzheimer's disease: understanding the paradigms, limitations, and contributions. Alzheimers Dement 5:340-347
77. Jiang X, Cheng H, Yang K, Gross RW, Han X (2007) Alkaline methanolysis of lipid extracts extends shotgun lipidomics analyses to the low abundance regime of cellular sphingolipids. Anal Biochem 371:135-145
78. Gearing M, Schneider JA, Robbins RS, Hollister RD, Mori H, Games D, Hyman BT, Mirra SS (1995) Regional variation in the distribution of apolipoprotein E and A beta in Alzheimer's disease. J Neuropathol Exp Neurol 54:833-841
79. Bales KR, Dodart JC, DeMattos RB, Holtzman DM, Paul SM (2002) Apolipoprotein E, amyloid, and Alzheimer disease. Mol Interv 2:363-375
80. Kang DE, Pietrzik CU, Baum L, Chevallier N, Merriam DE, Kounnas MZ, Wagner SL, Troncoso JC, Kawas CH, Katzman R, Koo EH (2000) Modulation of amyloid beta-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. J Clin Invest 106:1159-1166
81. Kuo YM, Crawford F, Mullan M, Kokjohn TA, Emmerling MR, Weller RO, Roher AE (2000) Elevated A beta and apolipoprotein E in A betaPP transgenic mice and its relationship to amyloid accumulation in Alzheimer's disease. Mol Med 6:430-439
82. Michikawa M (2003) Cholesterol paradox: is high total or low HDL cholesterol level a risk for Alzheimer's diseasé J Neurosci Res 72:141-146
83. Martins IJ, Hone E, Foster JK, Sunram-Lea SI, Gnjec A, Fuller SJ, Nolan D, Gandy SE, Martins RN (2006) Apolipoprotein E, cholesterol metabolism, diabetes, and the convergence of risk factors for Alzheimer's disease and cardiovascular disease. Mol Psychiatry 11:721-736
84. Nichol K, Deeny SP, Seif J, Camaclang K, Cotman CW (2009) Exercise improves cognition and hippocampal plasticity in APOE epsilon4 mice. Alzheimers Dement 5:287-294