The role of apolipoprotein e in neurodegeneration and cardiovascular disease

Expert Review of Proteomics

Volumn 11, Issue 3, 2014, Pages 371-381

  Lopez, Mary F ^a   Krastins, Bryan ^a   Ning, Mingming ^b  

^a Thermo Fisher Scientific   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Alzheimer's disease; apolipoprotein E; cardiovascular disease; mass spectrometry; stroke

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E2; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; ISOPROTEIN;

ALLELE; CARDIOVASCULAR DISEASE; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; DOWN SYNDROME; GENETIC VARIABILITY; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HUMAN; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEASUREMENT; NERVE DEGENERATION; NEUROPATHOLOGY; PREECLAMPSIA; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; ALZHEIMER DISEASE; DEGENERATIVE DISEASE; GENETICS; METABOLISM; PROTEOMICS;

ALZHEIMER DISEASE; APOLIPOPROTEINS E; CARDIOVASCULAR DISEASES; HUMANS; NEURODEGENERATIVE DISEASES; PROTEIN ISOFORMS; PROTEOMICS;

EID: 84901056499     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1586/14789450.2014.901892     Document Type: Review

References (93)

1. Zannis VI, McPherson J, Goldberger G, et al. Synthesis, intracellular processing, and signal peptide of human apolipoprotein E. J Biol Chem 1984;259:5495-9
2. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988;240(4852): 622-30
3. The UniProt Consortium Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucl Acid Res 2013.41: D43-7. Available from: www.uniprot.org/uniprot/P 026 49
4. Emi M, Wu LL, Robertson MA, et al. Genotyping and sequence analysis of apolipoprotein E isoforms. Genomics 1988;3:373-9
5. Szklarczyk D, Franceschini A, Kuhn M, et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011;39: D561-8
6. STRING-known and predicted protein-protein interactions. Available from: http://string-db.org
7. Mahley RW, Weisgraber KH, Huang Y. Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS. J Lipid Res 2009;50:S183-8
8. Leroy A, Landrieu I, Huvent I, et al. Spectroscopic studies of GSK3{beta} phosphorylation of the neuronal tau protein and its interaction with the N-terminal domain of apolipoprotein E. J Biol Chem 2010;285:33435-44
9. Kang J, Albadawi H, Patel VI, et al. Apolipoprotein E-/-mice have delayed skeletal muscle healing after hind limb ischemia-reperfusion. J Vasc Surg 2008;48: 701-8
10. Chuang K, Elford EL, Tseng J, et al. An expanding role for apolipoprotein E in sepsis and inflammation. Am J Surg 2010;200:391-7
11. Fu P, Wang AM, He LY, et al. Elevated serum ApoE levels are associated with bacterial infections in pediatric patients. J Microbiol Immunol Infect 2013. [Epub ahead of print]
12. Eisenberg DT, Kuzawa CW, Hayes MG. Worldwide allele frequencies of the human apolipoprotein E gene: climate, local adaptations, and evolutionary history. Am J Phys Anthropol 2010;143: 100-11
13. Weisgraber KH, Innerarity TL, Mahley RW. Abnormal lipoprotein receptor-binding activity of the human E apoprotein due to cysteine-arginine interchange at a single site. J Biol Chem 1982;257:2518-21
14. Corbo RM, Scacchi R. Apolipoprotein E (APOE) allele distribution in the world. Is APOE4 a "thrifty" allele? Ann Hum Genet 1999;43:1657-9
15. Ghebranious N, Ivacic L, Mallum J, Dokken C. Detection of ApoE E2, E3 and E4 alleles using MALDI-TOF mass spectrometry and the homogeneous mass-extend technology. Nucleic Acids Res 2005;33:e149
16. Breslow JL, Zannis VI, SanGiacomo TR, et al. Studies of familial type III hyperlipoproteinemia using as a genetic marker the apoE phenotype E2/2. J Lipid Res 1982;23:1224-35
17. Civeira F, Pocovi M, Cenarro A, et al. Apo E variants in patients with type III hyperlipoproteinemia. Atherosclerosis 1996; 127:273-82
18. Feussner G, Feussner V, Hoffmann MM, et al. Molecular basis of type III hyperlipoproteinemia in Germany. Hum Mutat 1998;11:417-23
19. Davignon J, Gregg RE, Sing CF. Apolipoprotein E polymorphism and atherosclerosis. Arteriosclerosis 1988;8:1-21
20. Huang X, Chen PC, Poole C. APOE-[epsilon]2 allele associated with higher prevalence of sporadic Parkinson disease. Neurology 2004;62:2198-202
21. Corder EH, Saunders AM, Strittmatter WJ, et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993; 261(5123):921-3
22. Strittmatter WJ, Saunders AM, Schmechel D, et al. 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 1993;90:1977-81
23. Farlow MR, He Y, Tekin S, et al. Impact of APOE in mild cognitive impairment. Neurology 2004;63:1898-901
24. Deary IJ, Whiteman MC, Pattie A, et al. Cognitive change and the APOE epsilon allele. Nature 2002;418(6901):932
25. Raber J. AR, apoE, and cognitive function. Horm Behav 2008;53:706-15
26. Friedman G, Froom P, Sazbon L, et al. Apolipoprotein E-epsilon4 genotype predicts a poor outcome in survivors of traumatic brain injury. Neurology 1999;52:244-8
27. McCarron MO, Delong D, Alberts MJ. APOE genotype as a risk factor for ischemic cerebrovascular disease: a meta-analysis. Neurology 1999;53:1308-11
28. Chapman J, Vinokurov S, Achiron A, et al. APOE genotype is a major predictor of long-term progression of disability in MS. Neurology 2001;56:312-16
29. Schmidt S, Barcellos LF, DeSombre K, et al. Multiple Sclerosis Genetics Group Association of polymorphisms in the apolipoprotein E region with susceptibility to and progression of multiple sclerosis. Am J Hum Gen 2002;70:708-17
30. Kadotani H, Kadotani T, Young T, et al. Association between apolipoprotein E epsilon4 and sleep-disordered breathing in adults. JAMA 2001;285:2888-90
31. Gottlieb DJ, DeStefano AL, Foley DJ, et al. APOE epsilon4 is associated with obstructive sleep apnea/hypopnea: the Sleep Heart Health Study. Neurology 2004;63: 664-8
32. Burt TD, Agan BK, Marconi VC, et al. Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE epsilon4/epsilon4 genotype accelerates HIV disease progression. Proc Natl Acad Sci USA 2008;105:8718-23
33. Chen J, Li Q, Wang J. Topology of human apolipoprotein E3 uniquely regulates its diverse biological functions. Proc Natl Acad Sci USA 2011;108:14813-18
34. Zhong N, Scearce-Levie K, Ramaswamy G, Weisgraber KH. Apolipoprotein E4 domain interaction. Synaptic and cognitive deficits in mice. Alzheimers Dement 2008;4:179-92
35. Farrer LA, Cupples LA, Haines JL, et al. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA 1997;278:1349-56
36. Frisardi V. Apolipoprotein E genotype: the innocent bystander or active bridge between metabolic syndrome and cognitive impairment? J Alzheimers Dis 2012; 30(Suppl 2):S283-304
37. Zlokovic BV. Cerebrovascular effects of apolipoprotein E: implications for Alzheimer disease. JAMA Neurol 2013;70:440-4
38. Silva T, Teixeira J, Remiao F, Borges F. Alzheimer's disease, cholesterol, and statins: the junctions of important metabolic pathways. Angew Chem Int Ed Engl 2013;52:1110-21
39. Rhinn H, Fujita R, Qiang L, et al. Integrative genomics identifies APOE e4 effectors in Alzheimer's disease. Nature 2013;500(7460):45-50
40. Ringman JM, Coppola G. New genes and new insights from old genes: update on Alzheimer disease. Continuum (N Y) 2013;19:358-71
41. Carlo AS. Sortilin, a novel APOE receptor implicated in Alzheimer disease. Prion 2013;7(5):378-82
42. Wolf AB, Caselli RJ, Reiman EM, Valla J. APOE and neuroenergetics: an emerging paradigm in Alzheimer's disease. Neurobiol Aging 2013;34:1007-17
43. Reitz C. Dyslipidemia and the risk of Alzheimer's disease. Curr Atheroscler Rep 2013;15:307
44. Adeosun SO, Hou X, Zheng B, et al. Cognitive deficits and disruption of neurogenesis in a mouse model of apolipoprotein e4 domain interaction. J Biol Chem 2014;289:2946-59
45. Raffai RL, Dong LM, Farese RV Jr, Weisgraber KH. Introduction of human apolipoprotein E4 "domain interaction" into mouse apolipoprotein E. Proc Natl Acad Sci USA 2001;98:11587-91
46. Zhong N, Scearce-Levie K, Ramaswamy G, Weisgraber KH. Apolipoprotein E4 domain interaction. Synaptic and cognitive deficits in mice. Alzheimers Dement 2008;4:179-92
47. Alamed J, Wilcock D M, Diamond D M, et al. Two-day radial-arm water maze learning and memory task. Robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 2006;1:1671-9
48. Dellu F, Mayo W, Cherkaoui J, et al. A two-trial memory task with automated recording. Study in young and aged rats. Brain Res 1992;588:132-9
49. Vuillermot S, Joodmardi E, Perlmann T, et al. Schizophrenia-relevant behaviors in a genetic mouse model of constitutive Nurr1 deficiency. Genes Brain Behav 2011;10:589-603
50. Wright RL, Conrad CD. Chronic stress leaves novelty seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005;8:151-4
51. Akanmu MA, Adeosun SO, Ilesanmi OR. Neuropharmacological effects of oleamide in male and female mice. Behav Brain Res 2007;182:88-94
52. Holcomb LA, Gordon MN, Jantzen P, et al. Behavioral changes in transgenic mice expressing both amyloid precursor protein and presenilin-1 mutations. Lack of association with amyloid deposits. Behav Genet 1999;29:177-85
53. Ramonet D, Daher J P, Lin B M, et al. Dopaminergic neuronal loss, reduced neurite complexity and autophagic abnormalities in transgenic mice expressing G2019S mutant LRRK2. PLoS One 2011;6:e18568
54. Adeosun SO, Hou X, Jiao Y, et al. Allopregnanolone reinstates tyrosine hydroxylase immunoreactive neurons and motor performance in an MPTP-lesioned mouse model of Parkinson's disease. PLoS One 2012;7:e50040
55. West HL, Rebeck GW, Hyman BT. Frequency of the apolipoprotein E epsilon 2 allele is diminished in sporadic Alzheimer disease. Neurosci Lett 1994;175:46-8
56. Benjamin R, Leake A, McArthur FK, et al. Protective effect of apoE epsilon 2 in Alzheimer's disease. Lancet 1994;344:473
57. Nagy Z, Esiri MM, Jobst KA, et al. Influence of the apolipoprotein E genotype on amyloid deposition and neurofibrillary tangle formation in Alzheimer's disease. Neuroscience 1995;69:757-61
58. Hostage CA, Roy Choudhury K, Doraiswamy PM, Petrella JR. Alzheimer's Disease Neuroimaging Initiative. Dissecting the gene dose-effects of the APOE e4 and e2 alleles on hippocampal volumes in aging and Alzheimer's disease. PLoS One 2013; 8(2):e54483
59. Hendriks L, van Duijn CM, Cras P, et al. Presenile demetia and cerebral haemorrhage linked to a mutation at codon 692 of the b-amyloid precursor protein gene. Nat Genetics 1992;1:218-21
60. Grabowski TJ, Cho HS, Vonsattel JP, et al. Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann Neurol 2001;49:697-705
61. Greenberg SM, Eng JA, Ning M, et al. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke 2004;35:1415-2015
62. O'Donnell HC, Rosand J, Knudsen KA, et al. Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 2000;342:240-5
63. Yamada M. Brain hemorrhages in cerebral amyloid angiopathy. Semin Thromb Hemost 2013;39:955-62
64. Rannikmae K, Samarasekera N, Mart̂inez-Gonzalez NA, et al. Genetics of cerebral amyloid angiopathy: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2013;84:901-8
65. Rengifo L, Gaviria D, Serrano H. APOE gene polymorphisms associated with Down syndrome in Colombian populations. Biomedica 2012;32:224-32
66. Lott IT, Head E. Alzheimer disease and Down syndrome: factors in pathogenesis. Neurobiol Aging 2005;26:383-9
67. Jones EL, Mok K, Hanney M, et al. Evidence that PICALM affects age at onset of Alzheimer's dementia in Down syndrome. Neurobiol Aging 2013;34:2441
68. Schilling S, DeStefano AL, Sachdev PS, et al. APOE genotype and MRI markers of cerebrovascular disease: systematic review and meta-analysis. Neurology 2013;81: 292-300
69. Anand SS, Xie C, Pare G, et al. Genetic ariants associated with myocardial infarction risk factors in over 8000 individuals from five ethnic groups: the INTERHEART Genetics Study. Circ Cardiovasc Genet 2009;2:16-25
70. Damani SB, Topol EJ. Emerging genomic applications in coronary artery disease. JACC Cardiovasc Interv 2011;4:473-82
71. Vegh C, Langmar Z, Szerzo M, et al. Connections between apolipoprotein E genotypes and the development of cardiovascular diseases. Orv Hetil 2012;153: 2070-6
72. Malygina NA, Kostomarova IV, Vodolagina NN, et al. The genes of atherosclerosis and cardiovascular diseases. Klin Med 2011;89:14-18
73. Kothapalli D, Liu SL, Bae YH, et al. Cardiovascular protection by ApoE and ApoE-HDL linked to suppression of ECM gene expression and arterial stiffening. Cell Rep 2012;29:1259-71
74. Atkinson KR, Blumenstein M, Black MA, et al. An altered pattern of circulating apolipoprotein E3 isoforms is implicated in preeclampsia. J Lipid Res 2009;50:71-80
75. Ahmadi R, Rahimi Z, Vaisi-Raygani A, et al. Apolipoprotein E genotypes, lipid peroxidation, and antioxidant status among mild and severe preeclamptic women from western Iran: protective role of apolipoprotein £2 allele in severe preeclampsia. Hypertens Pregnancy 2012;31:405-18
76. Utermann G, Jaeschke M, Menzel J. Familial hyperlipoproteinemia type III: deficiency of a specific apolipoprotein (apo E-III) in the very-low-density lipoproteins. FEBS Lett 1975;56:352-5
77. Nilsson J, Rueetschi U, Halim A, et al. Enrichment of glycopeptides for glycan structure and attachment site identification. Nat Methods 2009;6:809-11
78. Paik Y-K, Chang DJ, Reardon CA, et al. Nucleotide sequence and structure of the human apolipoprotein E gene. Proc Natl Acad Sci USA 1985;82:3445-9
79. Hixon JE, Vernier DT. Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 1990;31:545-8
80. Kontula K, Aalto-Setala K, Kuusi T, et al. Apolipoprotein E polymorphism determined by restriction enzyme analysis of DNA amplified by polymerase chain reaction: convenient alternative to phenotyping by isoelectric focusing. Clin Chem 1990;36:2087-92
81. Wenham PR, Price WH, Blundell G. Apolipoprotein E genotyping by one-stage PCR Lancet. 1991;337:1158-9
82. Zivelin A, Rosenberg N, Peretz H, et al. Improved method for genotyping apolipoprotein E polymorphisms by a PCR-based assay simultaneously utilizing two distinct restriction enzymes. Clin Chem 1997;43:1657-9
83. McLean JW, Elshourbagy NA, Chang DJ, et al. Human apolipoprotein E mRNA. cDNA cloning and nucleotide sequencing of a new variant. J Biol Chem 1984;259: 6498-504
84. de Knijff P, van den Maagdenberg AM, Frants RR, Havekes LM. Genetic heterogeneity of apolipoprotein E and its influence on plasma lipid and lipoprotein levels. Hum Mutat 1994;4:178-94
85. Nickerson DA, Taylor SL, Fullerton SM, et al. Sequence diversity and large-scale typing of SNPs in the human apolipoprotein E gene. Genome Res 2000;10:1532-45
86. Stengard JH, Clark AG, Weiss KM, et al. Contributions of 18 additional DNA sequence variations in the gene encoding apolipoprotein E to explaining variation in quantitative measures of lipid metabolism. Am J Hum Genet 2002;71:501-17
87. Nedelkov D, Kiernan UA, Niederkofler EE, et al. Investigating diversity in human plasma proteins. Proc Natl Acad Sci USA 2005;102:10852-7
88. Wildsmith KR, Han B, Bateman RJ. Method for the simultaneous quantitation of apolipoprotein E isoforms using tandem mass spectrometry. Anal Biochem 2009;395:116-18
89. Krastins B, Prakash A, Sarracino DA, et al. Rapid development of sensitive, high-throughput, quantitative and highly selective mass spectrometric targeted immunoassays for clinically important proteins in human plasma and serum. Clin Biochem 2013;46:399-410
90. Mart́inez-Morillo E, Nielsen HM, Batruch I, et al. Assessment of peptide chemical modifications on the development of an accurate and precise multiplex selected reaction monitoring assay for Apolipoprotein E isoforms. J Proteom Res 2014;13(2): 1077-87
91. Lopez MF, Sarracino DA, Prakash A, et al. Discrimination of ischemic and hemorrhagic strokes using a multiplexed, mass spectrometry-based assay for serum apolipoproteins coupled to multi-marker ROC algorithm. Proteomics Clin Appl 2012;6:190-200
92. Biffi A, Anderson CD, Jagiella JM, et al. APOE genotype and extent of bleeding and outcome in lobar intracerebral haemorrhage: a genetic association study. Lancet Neurol 2011;10:702-9
93. 3D Macromolecular Structures. Available from: www.ncbi.nlm.nih.gov/ structure/MMDB/mmdb.shtml