ApoE4 upregulates the activity of mitochondria-associated ER membranes

EMBO Reports

Volumn 17, Issue 1, 2016, Pages 27-36

  Tambini, Marc D ^a   Pera, Marta ^a   Kanter, Ellen ^a   Yang, Hua ^a   Guardia Laguarta, Cristina ^a   Holtzman, David ^b   Sulzer, David ^a   Area Gomez, Estela ^a   Schon, Eric A ^a  

^a New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ApoE; cholesterol; cholesteryl esters; endoplasmic reticulum; lipoproteins; MAM; mitochondria; phospholipids

Indexed keywords

APOLIPOPROTEIN A4; CHOLESTEROL ESTER; PHOSPHOLIPID; APOLIPOPROTEIN E4; CHOLESTEROL; CONDITIONED MEDIUM; LIPOPROTEIN;

ALZHEIMER DISEASE; ARTICLE; ASTROCYTE CONDITIONED MEDIUM; CULTURE MEDIUM; ENDOPLASMIC RETICULUM MEMBRANE; GENETIC RISK; LIPID HOMEOSTASIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOLECULAR PATHOLOGY; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RISK FACTOR; UPREGULATION; ANIMAL; ASTROCYTE; BIOSYNTHESIS; CHEMISTRY; CONDITIONED MEDIUM; ENDOPLASMIC RETICULUM; GENETICS; HUMAN; INTRACELLULAR MEMBRANE; LIPID METABOLISM; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSCRIPTION INITIATION;

ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E4; ASTROCYTES; CHOLESTEROL; CHOLESTEROL ESTERS; CULTURE MEDIA, CONDITIONED; ENDOPLASMIC RETICULUM; HUMANS; INTRACELLULAR MEMBRANES; LIPID METABOLISM; LIPOPROTEINS; MICE; MITOCHONDRIA; PHOSPHOLIPIDS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84955350049     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540614     Document Type: Article

References (70)

1. Goedert M, Spillantini MG, (2006) A century of Alzheimer's disease. Science 314: 777-781
2. Pani A, Dessì S, Diaz G, La Colla P, Abete C, Mulas C, Angius F, Cannas MD, Orru CD, Cocco PL, et al, (2009) Altered cholesterol ester cycle in skin fibroblasts from patients with Alzheimer's disease. J Alzheimers Dis 18: 829-841
3. Stefani M, Liguri G, (2009) Cholesterol in Alzheimer's disease: unresolved questions. Curr Alz Res 6: 15-29
4. Pettegrew JW, Panchalingam K, Hamilton RL, McClure RJ, (2001) Brain membrane phospholipid alterations in Alzheimer's disease. Neurochem Res 26: 771-782
5. Bezprozvanny I, Mattson MP, (2008) Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends Neurosci 31: 454-463
6. Wang X, Su B, Zheng L, Perry G, Smith MA, Zhu X, (2009) The role of abnormal mitochondrial dynamics in the pathogenesis of Alzheimer's disease. J Neurochem 109: 153-159
7. Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, Guardia-Laguarta C, de Groof AJC, Madra M, Ikenouchi J, Umeda M, Bird TD, Sturley SL, et al, (2012) Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J 31: 4106-4123
8. Hayashi T, Fujimoto M, (2010) Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol Pharmacol 77: 517-528
9. Williamson CD, Zhang A, Colberg-Poley AM, (2011) The human cytomegalovirus protein UL37 exon 1 associates with internal lipid rafts. J Virol 85: 2100-2111
10. Area-Gomez E, de Groof AJ, Boldogh I, Bird TD, Gibson GE, Koehler CM, Yu WH, Duff KE, Yaffe MP, Pon LA, et al, (2009) Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria. Am J Pathol 175: 1810-1816
11. Schon EA, Area-Gomez E, (2010) Is Alzheimer's disease a disorder of mitochondria-associated membranes? J Alzheimers Dis 20 (Suppl 2): S281-S292
12. Schon EA, Area-Gomez E, (2013) Mitochondria-associated ER membranes in Alzheimer disease. Mol Cell Neurosci 55: 26-36
13. Tanzi RE, (2012) The genetics of Alzheimer disease. Cold Spring Harb Perspect Med 2: a006296
14. Holtzman DM, Herz J, Bu G, (2012) Apolipoprotein E and apolipoprotein E receptors: normal biology and roles in Alzheimer disease. Cold Spring Harb Perspect Med 2: a006312
15. Lund-Katz S, Phillips MC, (2010) High density lipoprotein structure-function and role in reverse cholesterol transport. Subcell Biochem 51: 183-227
16. Pitas RE, Boyles JK, Lee SH, Foss D, Mahley RW, (1987) Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim Biophys Acta 917: 148-161
17. Gerdes LU, (2003) The common polymorphism of apolipoprotein E: geographical aspects and new pathophysiological relations. Clin Chem Lab Med 41: 628-631
18. Farrer LA, Cupples LA, Haines JL, Hyman B, Kukull WA, Mayeux R, Myers RH, Pericak-Vance MA, Risch N, van Duijn CM, (1997) Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. JAMA 278: 1349-1356
19. DeMattos RB, Rudel LL, Williams DL, (2001) Biochemical analysis of cell-derived apoE3 particles active in stimulating neurite outgrowth. J Lipid Res 42: 976-987
20. Hayashi H, Campenot RB, Vance DE, Vance JE, (2007) Apolipoprotein E-containing lipoproteins protect neurons from apoptosis via a signaling pathway involving low-density lipoprotein receptor-related protein-1. J Neurosci 27: 1933-1941
21. Xu Q, Bernardo A, Walker D, Kanegawa T, Mahley RW, Huang Y, (2006) Profile and regulation of apolipoprotein E (ApoE) expression in the CNS in mice with targeting of green fluorescent protein gene to the ApoE locus. J Neurosci 26: 4985-4994
22. Harris FM, Tesseur I, Brecht WJ, Xu Q, Mullendorff K, Chang S, Wyss-Coray T, Mahley RW, Huang Y, (2004) Astroglial regulation of apolipoprotein E expression in neuronal cells. Implications for Alzheimer's disease. J Biol Chem 279: 3862-3868
23. Ramaswamy G, Xu Q, Huang Y, Weisgraber KH, (2005) Effect of domain interaction on apolipoprotein E levels in mouse brain. J Neurosci 25: 10658-10663
24. Ulrich JD, Burchett JM, Restivo JL, Schuler DR, Verghese PB, Mahan TE, Landreth GE, Castellano JM, Jiang H, Cirrito JR, et al, (2013) In vivo measurement of apolipoprotein E from the brain interstitial fluid using microdialysis. Mol Neurodegen 8: 13
25. Voelker DR, (2005) Bridging gaps in phospholipid transport. Trends Biochem Sci 30: 396-404
26. Hayashi T, Rizzuto R, Hajnoczky G, Su TP, (2009) MAM: more than just a housekeeper. Trends Cell Biol 19: 81-88
27. Vance JE, (2008) Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J Lipid Res 49: 1377-1387
28. Gibellini F, Smith TK, (2010) The Kennedy pathway-De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62: 414-428
29. Schumacher MM, Choi JY, Voelker DR, (2002) Phosphatidylserine transport to the mitochondria is regulated by ubiquitination. J Biol Chem 277: 51033-51042
30. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC, (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200
31. de Brito OM, Scorrano L, (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456: 605-610
32. Makino A, Baba T, Fujimoto K, Iwamoto K, Yano Y, Terada N, Ohno S, Sato SB, Ohta A, Umeda M, et al, (2003) Cinnamycin (Ro 09-0198) promotes cell binding and toxicity by inducing transbilayer lipid movement. J Biol Chem 278: 3204-3209
33. Marki F, Hanni E, Fredenhagen A, van Oostrum J, (1991) Mode of action of the lanthionine-containing peptide antibiotics duramycin, duramycin B and C, and cinnamycin as indirect inhibitors of phospholipase A2. Biochem Pharmacol 42: 2027-2035
34. Heeren J, Grewal T, Laatsch A, Becker N, Rinninger F, Rye K-A, Beisiegel U, (2004) Impaired recycling of apolipoprotein E4 is associated with intracellular cholesterol accumulation. J Biol Chem 279: 55483-55492
35. Heeren J, Grewal T, Laatsch A, Rottke D, Rinninger F, Enrich C, Beisiegel U, (2003) Recycling of apoprotein E is associated with cholesterol efflux and high density lipoprotein internalization. J Biol Chem 278: 14370-14378
36. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, Smith JD, Ladu MJ, Rostagno A, et al, (2000) Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 348 (Pt 2): 359-365
37. Rusinol AE, Cui Z, Chen MH, Vance JE, (1994) A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. J Biol Chem 269: 27494-27502
38. Puglielli L, Konopka G, Pack-Chung E, Ingano LA, Berezovska O, Hyman BT, Chang TY, Tanzi RE, Kovacs DM, (2001) Acyl-coenzyme A: cholesterol acyltransferase modulates the generation of the amyloid β-peptide. Nat Cell Biol 3: 905-912
39. Puglielli L, Ellis BC, Ingano LA, Kovacs DM, (2004) Role of acyl-coenzyme A:cholesterol acyltransferase activity in the processing of the amyloid precursor protein. J Mol Neurosci 24: 93-96
40. Gõmez-Ramos P, Asunciõn Morán M, (2007) Ultrastructural localization of intraneuronal Aβ-peptide in Alzheimer disease brains. J Alzheimers Dis 11: 53-59
41. Bottinger L, Horvath SE, Kleinschroth T, Hunte C, Daum G, Pfanner N, Becker T, (2012) Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J Mol Biol 423: 677-686
42. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD, (1993) Apolipoprotein E: high-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90: 1977-1981
43. Sagare AP, Bell RD, Srivastava A, Sengillo JD, Singh I, Nishida Y, Chow N, Zlokovic BV, (2013) A lipoprotein receptor cluster IV mutant preferentially binds amyloid-β and regulates its clearance from the mouse brain. J Biol Chem 288: 15154-15166
44. Vincent B, Smith JD, (2001) Astrocytes down-regulate neuronal β-amyloid precursor protein expression and modify its processing in an apolipoprotein E isoform-specific manner. Eur J Neurosci 14: 256-266
45. Verghese PB, Castellano JM, Garai K, Wang Y, Jiang H, Shah A, Bu G, Frieden C, Holtzman DM, (2013) ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions. Proc Natl Acad Sci USA 110: E1807-E1816
46. Harris FM, Brecht WJ, Xu Q, Tesseur I, Kekonius L, Wyss-Coray T, Fish JD, Masliah E, Hopkins PC, Scearce-Levie K, et al, (2003) Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc Natl Acad Sci USA 100: 10966-10971
47. Guo L, LaDu MJ, Van Eldik LJ, (2004) A dual role for apolipoprotein E in neuroinflammation: anti- and pro-inflammatory activity. J Mol Neurosci 23: 205-212
48. Bell RD, Winkler EA, Singh I, Sagare AP, Deane R, Wu Z, Holtzman DM, Betsholtz C, Armulik A, Sallstrom J, et al, (2012) Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature 485: 512-516
49. Di Paolo G, Kim T-W, (2011) Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat Rev Neurosci 12: 284-296
50. Pierrot N, Tyteca D, D'Auria L, Dewachter I, Gailly P, Hendrickx A, Tasiaux B, Haylani LE, Muls N, N'Kuli F, et al, (2013) Amyloid precursor protein controls cholesterol turnover needed for neuronal activity. EMBO Mol Med 5: 608-625
51. Schneider A, Rajendran L, Honsho M, Gralle M, Donnert G, Wouters F, Hell SW, Simons M, (2008) Flotillin-dependent clustering of the amyloid precursor protein regulates its endocytosis and amyloidogenic processing in neurons. J Neurosci 28: 2874-2882
52. Sparks DL, Scheff SW, Hunsaker JC 3rd, Liu H, Landers T, Gross DR, (1994) Induction of Alzheimer-like β-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol. Exp Neurol 126: 88-94
53. Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM, Hadziselimovic A, Beel AJ, Sanders CR, (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336: 1168-1171
54. Beel AJ, Mobley CK, Kim HJ, Tian F, Hadziselimovic A, Jap B, Prestegard JH, Sanders CR, (2008) Structural studies of the transmembrane C-terminal domain of the amyloid precursor protein (APP): does APP function as a cholesterol sensor? Biochemistry 47: 9428-9446
55. Marquer C, Devauges V, Cossec J-C, Liot G, Lecart S, Saudou F, Duyckaerts C, Leveque-Fort S, Potier M-C, (2011) Local cholesterol increase triggers amyloid precursor protein-Bace1 clustering in lipid rafts and rapid endocytosis. FASEB J 25: 1295-1305
56. Urano Y, Hayashi I, Isoo N, Reid PC, Shibasaki Y, Noguchi N, Tomita T, Iwatsubo T, Hamakubo T, Kodama T, (2005) Association of γ-secretase complex with lipid rafts. J Lipid Res 46: 904-912
57. Bodovitz S, Klein WL, (1996) Cholesterol modulates α-secretase cleavage of amyloid precursor protein. J Biol Chem 271: 4436-4440
58. Wirz KTS, Keitel S, Swaab DF, Verhaagen J, Bossers K, (2014) Early molecular changes in Alzheimer disease: can we catch the disease in its presymptomatic phase? J Alzheimers Dis 38: 719-740
59. McIntosh AM, Bennett C, Dickson D, Anestis SF, Watts DP, Webster TH, Fontenot MB, Bradley BJ, (2012) The apolipoprotein E (APOE) gene appears functionally monomorphic in chimpanzees (Pan troglodytes). PLoS ONE 7: e47760
60. 2+ transfer in the control of apoptosis. Oncogene 27: 6407-6418
61. Roselaar SE, Daugherty A, (1998) Apolipoprotein E-deficient mice have impaired innate immune responses to Listeria monocytogenes in vivo. J Lipid Res 39: 1740-1743
62. Martin GM, (1999) APOE alleles and lipophylic pathogens. Neurobiol Aging 20: 441-443
63. Cloonan SM, Choi AMK, (2013) Mitochondria: sensors and mediators of innate immune receptor signaling. Curr Opin Microbiol 16: 327-338
64. Vieira FS, Correa G, Einicker-Lamas M, Coutinho-Silva R, (2010) Host-cell lipid rafts: a safe door for micro-organisms? Biol Cell 102: 391-407
65. Price DA, Bassendine MF, Norris SM, Golding C, Toms GL, Schmid ML, Morris CM, Burt AD, Donaldson PT, (2006) Apolipoprotein ε3 allele is associated with persistent hepatitis C virus infection. Gut 55: 715-718
66. Xu PT, Schmechel D, Rothrock-Christian T, Burkhart DS, Qiu HL, Popko B, Sullivan P, Maeda N, Saunders AM, Roses AD, et al, (1996) Human apolipoprotein E2, E3, and E4 isoform-specific transgenic mice: human-like pattern of glial and neuronal immunoreactivity in central nervous system not observed in wild-type mice. Neurobiol Dis 3: 229-245
67. Fagan AM, Holtzman DM, Munson G, Mathur T, Schneider D, Chang LK, Getz GS, Reardon CA, Lukens J, Shah JA, et al, (1999) Unique lipoproteins secreted by primary astrocytes from wild type, apoE (-/-), and human apoE transgenic mice. J Biol Chem 274: 30001-30007
68. Staal RGW, Rayport S, Sulzer D, (2007) Amperometric detection of dopamine exocytosis from synaptic terminals. In Electrochemical Methods for Neuroscience, Michael AC, Borland M, (eds), pp 340-349. Boca Raton, FL: CRC Press
69. Saifer A, Goldman L, (1961) The free fatty acids bound to human serum albumin. J Lipid Res 2: 268-270
70. Vance JE, Hayashi H, (2010) Formation and function of apolipoprotein E-containing lipoproteins in the nervous system. Biochim Biophys Acta 1801: 806-818