Annexins as organizers of cholesterol- and sphingomyelin-enriched membrane microdomains in Niemann-Pick type C disease

Cellular and Molecular Life Sciences

Volumn 69, Issue 11, 2012, Pages 1773-1785

  Domon, Magdalena ^a,b,c,d,e,f   Nasir, Mehmet Nail ^b,c,d,e,f   Matar, Gladys ^b,c,d,e,f   Pikula, Slawomir ^a   Besson, Françoise ^b,c,d,e,f   Bandorowicz Pikula, Joanna ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITÉ DE LYON   (France)

^e CPE LYON   (France)

^f UNIVERSITÉ LYON 1   (France)

Author keywords

Annexins; Cholesterol; Membrane microdomains; Niemann Pick type C disease

Indexed keywords

ANNEXIN; CALPHOBINDIN II; CHOLESTEROL; LIPOCORTIN 2; SPHINGOMYELIN;

BINDING AFFINITY; CELL DEATH; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; ENDOPLASMIC RETICULUM; GENE; GENE MUTATION; HUMAN; LIPID RAFT; MEMBRANE STRUCTURE; NIEMANN PICK DISEASE; NONHUMAN; NPC2 GENE; PATHOGENESIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; REVIEW;

AMINO ACID SEQUENCE; ANNEXINS; CHOLESTEROL; HUMANS; MEMBRANE MICRODOMAINS; MOLECULAR SEQUENCE DATA; NIEMANN-PICK DISEASE, TYPE C; SEQUENCE ALIGNMENT; SPHINGOMYELINS;

EID: 84862888460     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0894-0     Document Type: Review

References (139)

1. B Ramjiawan MP Czubryt JS Gilchrist GN Pierce 1996 Nuclear membrane cholesterol can modulate nuclear nucleoside triphosphatase activity J Cell Biochem 63 442 452 8978460 1:CAS:528:DyaK2sXhtVKksw%3D%3D (Pubitemid 27009264)
2. S Reineri A Bertoni E Sanna S Baldassarri C Sarasso M Zanfa I Canobbio M Torti F Sinigaglia 2007 Membrane lipid rafts coordinate estrogen-dependent signaling in human platelets Biochim Biophys Acta 1773 273 278 17208317 1:CAS:528:DC%2BD2sXhtVChtLY%3D (Pubitemid 46123621)
3. B Batetta F Sanna 2006 Cholesterol metabolism during cell growth: which role for the plasma membrane? Eur J Lipid Sci Technol 108 687 699 1:CAS:528:DC%2BD28Xpt1eitL0%3D (Pubitemid 44342547)
4. JP Liu Y Tang S Zhou BH Toh C McLean H Li 2010 Cholesterol involvement in the pathogenesis of neurodegenerative diseases Mol Cell Neurosci 43 33 42 19660552 1:CAS:528:DC%2BD1MXhs1Wgu7bE
5. T Grewal M Koese C Rentero C Enrich 2010 Annexin A6-regulator of the EGFR/Ras signalling pathway and cholesterol homeostasis Int J Biochem Cell Biol 42 580 584 20044025 1:CAS:528:DC%2BC3cXivFGrurs%3D
6. 2+ signaling with cholesterol transport Biochim Biophys Acta 1813 935 947 20888375 1:CAS:528:DC%2BC3MXkvFagtro%3D
7. T Harder R Kellner RG Parton J Gruenberg 1997 Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol Mol Biol Cell 8 533 545 9188103 1:CAS:528: DyaK2sXit1yrsLo%3D (Pubitemid 27171300)
8. Oliferenko S, Paiha K, Harder T, Gerke V, Schwärzler C, Schwarz H, Beug H, Günthert U, Huber LA (1999) Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J Cell Biol 146:843-854
9. 2+-regulated association of lipid microdomains J Cell Biol 150 1113 1124 10973999 1:CAS:528:DC%2BD3cXmtlegtL0%3D
10. EB Babiychuk A Draeger 2006 Biochemical characterization of detergent-resistant membranes: a systematic approach Biochem J 397 407 416 16608442 1:CAS:528:DC%2BD28XmvFakurw%3D (Pubitemid 44187499)
11. E Carafoli 2010 The fateful encounter of mitochondria with calcium: how did it happen? Biochim Biophys Acta 1797 595 606 20385096 1:CAS:528: DC%2BC3cXnvV2qsrk%3D
12. Haiech J, Audran E, Fève M, Ranjeva R, Kilhoffer MC (2011) Revisiting intracellular calcium signaling semantics. Biochimie 93:2029-2037
13. 2+ signalling to membrane dynamics Natl Rev Mol Cell Biol 6 449 461 1:CAS:528:DC%2BD2MXks1Gmtbo%3D (Pubitemid 40780557)
14. MA Lemmon 2008 Membrane recognition by phospholipid-binding domains Natl Rev Mol Cell Biol 9 99 111 1:CAS:528:DC%2BD1cXovFOntQ%3D%3D (Pubitemid 351158910)
15. V Gerke SE Moss 2002 Annexins: from structure to function Physiol Rev 82 331 371 11917092 1:CAS:528:DC%2BD38XjtFOns7c%3D (Pubitemid 34654456)
16. A Draeger K Monastyrskaya EB Babiychuk 2011 Plasma membrane repair and cellular damage control: the annexin survival kit Biochem Pharmcol 81 703 712 1:CAS:528:DC%2BC3MXit12jtLg%3D
17. CE Futter IJ White 2007 Annexins and endocytosis Traffic 8 951 958 17547702 1:CAS:528:DC%2BD2sXovVylurg%3D (Pubitemid 47074030)
18. MJ Hayes RE Longbottom MA Evans SE Moss 2007 Annexinopathies Subcell Biochem 45 1 28 18193632 1:STN:280:DC%2BD1c%2FktVahsA%3D%3D
19. LH Lim S Pervaiz 2007 Annexin 1: the new face of an old molecule FASEB J 21 968 975 17215481 1:CAS:528:DC%2BD2sXksVSqt7k%3D (Pubitemid 46495688)
20. L Fatimathas SE Moss 2010 Annexins as disease modifiers Histol Histopathol 25 527 532 20183805 1:CAS:528:DC%2BC3cXms1OkurY%3D
21. S Mukherjee FR Maxfield 2004 Lipid and cholesterol trafficking in NPC Biochim Biophys Acta 1685 28 37 15465424 1:CAS:528:DC%2BD2cXotFCksbk%3D (Pubitemid 39311808)
22. R Lindner HY Naim 2009 Domains in biological membranes Exp Cell Res 315 2871 2878 19632223 1:CAS:528:DC%2BD1MXht1aisL3L
23. Pike LJ (2009) The challenge of lipid rafts. J Lipid Res. 50 Suppl:S323-S328
24. YH Hao JW Chen 2001 Influence of cholesterol on the biophysical properties of the sphingomyelin/DOPC binary system J Membr Biol 183 85 92 11562790 1:CAS:528:DC%2BD3MXntFWiu78%3D
25. S Schuck K Simons 2004 Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane J Cell Sci 117 5955 5964 15564373 1:CAS:528:DC%2BD2MXnvFagsw%3D%3D (Pubitemid 40123962)
26. K Simons JL Sampaio 2011 Membrane organization and lipid rafts Cold Spring Harb Perspect Biol 3 a004697 21628426 1:CAS:528:DC%2BC38XhvFyksbs%3D
27. S Bonnin K El Kirat M Becchi M Dubois C Grangeasse C Giraud A-F Prigent M Lagarde B Roux F Besson 2003 Protein and lipid analysis of detergent-resistant membranes isolated from bovine kidney Biochimie 85 1237 1244 14739076 1:CAS:528:DC%2BD2cXltVKntg%3D%3D (Pubitemid 38096348)
28. U Coskun K Simons 2010 Membrane rafting: from apical sorting to phase segregation FEBS Lett 584 1685 1693 20036659 1:CAS:528:DC%2BC3cXkvFKqtbY%3D
29. Y Maeda T Kinoshita 2011 Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins Prog Lipid Res 50 411 424 21658410 1:CAS:528:DC%2BC3MXht1OisL%2FK
30. MC Giocondi F Besson P Dosset PE Milhiet C Le Grimellec 2007 Remodeling of ordered membrane domains by GPI-anchored intestinal alkaline phosphatase Langmuir 23 9358 9364 17661499 1:CAS:528:DC%2BD2sXot1ahs7g%3D (Pubitemid 47383525)
31. I Levental M Grzybek K Simons 2010 Greasing their way: lipid modifications determine protein association with membrane rafts Biochemistry 49 6305 6316 20583817 1:CAS:528:DC%2BC3cXos1ekur4%3D
32. Coskun U, Simons K (2011) Cell membranes: the lipid perspective. Structure 19:1543-1548
33. M Edidin 2003 The state of lipid rafts: from model membranes to cells Annu Rev Biophys Biomol Struct 32 257 283 12543707 1:CAS:528: DC%2BD3sXntFSgtr0%3D (Pubitemid 37056230)
34. SR Shaikh MA Edidin 2006 Membranes are not just rafts Chem Phys Lipids 144 1 3 16945359 1:CAS:528:DC%2BD28XhtVygsLbN (Pubitemid 44537270)
35. MB Shah PB Sehgal 2007 Nondetergent isolation of rafts Methods Mol Biol 398 21 28 18214371 1:CAS:528:DC%2BD2sXoslGrsLc%3D
36. DA Persaud-Sawin S Lightcap GJ Harry 2009 Isolation of rafts from mouse brain tissue by a detergent-free method J Lipid Res 50 759 767 19060326 1:CAS:528:DC%2BD1MXks1Witrg%3D
37. SR Wassall MR Brzustowicz SR Shaikh V Cherezov M Caffrey W Stillwell 2004 Order from disorder, corralling cholesterol with chaotic lipids. The role of polyunsaturated lipids in membrane raft formation Chem Phys Lipids 132 79 88 15530450 1:CAS:528:DC%2BD2cXpsFSktbg%3D (Pubitemid 39458322)
38. BM Castro LC Silva A Fedorov RF de Almeida M Prieto 2009 Cholesterol-rich fluid membranes solubilize ceramide domains: implications for the structure and dynamics of mammalian intracellular and plasma membranes J Biol Chem 284 22978 22987 19520848 1:CAS:528:DC%2BD1MXpvFKiurw%3D
39. van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI, Hubrich BE, Dier M, Hell SW, Grubmüller H, Diederichsen U, Jahn R (2011) Membrane protein sequestering by ionic protein-lipid interactions Nature 479:552-555
40. PJ Quinn C Wolf 2010 An X-ray diffraction study of model membrane raft structures FEBS J 277 4685 4698 20977668 1:CAS:528:DC%2BC3cXhsFSgtbvM
41. H Martinez-Seara T Róg M Karttunen I Vattulainen R Reigada 2010 Cholesterol induces specific spatial and orientational order in cholesterol/phospholipid membranes PLoS One 5 e11162 20567600
42. MN Nasir F Besson 2011 Specific interactions of mycosubtilin with cholesterol-containing artificial membranes Langmuir 27 10785 10792 21766869 1:CAS:528:DC%2BC3MXpsVOisLc%3D
43. A Björkbom T Róg K Kaszuba M Kurita S Yamaguchi M Lönnfors TK Nyholm I Vattulainen S Katsumura JP Slotte 2010 Effect of sphingomyelin headgroup size on molecular properties and interactions with cholesterol Biophys J 99 3300 3308 21081078
44. N Kahya 2010 Protein-protein and protein-lipid interactions in domain-assembly: lessons from giant unilamellar vesicles Biochim Biophys Acta 1798 1392 1398 20211599 1:CAS:528:DC%2BC3cXntVejs7Y%3D
45. S Banerji M Ngo CF Lane CA Robinson S Minogue ND Ridgway 2010 Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the Golgi apparatus requires phosphatidylinositol 4-kinase IIα Mol Biol Cell 21 4141 4150 20881054 1:CAS:528:DC%2BC3MXis1Oltg%3D%3D
46. C Bonnon MW Wendeler JP Paccaud HP Hauri 2010 Selective export of human GPI-anchored proteins from the endoplasmic reticulum J Cell Sci 123 1705 1715 20427317 1:CAS:528:DC%2BC3cXotFGrsb4%3D
47. Hummel I Klappe K, Ercan C, Kok JW (2011) Multidrug resistance-related protein 1 (MRP1) function and localization depend on cortical actin. Mol Pharmacol 79:229-240
48. RD Lasley 2011 Adenosine receptors and membrane microdomains Biochim Biophys Acta 1808 1284 1289 20888790 1:CAS:528:DC%2BC3MXjvFSrsr4%3D
49. C Zhang PL Li 2010 Membrane raft redox signalosomes in endothelial cells Free Radic Res 44 831 842 20528560 1:CAS:528:DC%2BC3cXhtVClu7zI
50. C Dart 2010 Lipid microdomains and the regulation of ion channel function J Physiol 588 3169 3178 20519314 1:CAS:528:DC%2BC3cXhtF2rur7O
51. SB Ganapathi TE Fox M Kester KS Elmslie 2010 Ceramide modulates HERG potassium channel gating by translocation into lipid rafts Am J Physiol Cell Physiol 299 C74 C86 20375276 1:CAS:528:DC%2BC3cXpslSgs7Y%3D
52. WR Sones AJ Davis N Leblanc IA Greenwood 2010 Cholesterol depletion alters amplitude and pharmacology of vascular calcium-activated chloride channels Cardiovasc Res 87 476 484 20172862 1:CAS:528:DC%2BC3cXptVylu78%3D
53. J Woudenberg KP Rembacz M Hoekstra A Pellicoro FA van den Heuvel J Heegsma SC van Ijzendoorn A Holzinger T Imanaka H Moshage KN Faber 2010 Lipid rafts are essential for peroxisome biogenesis in HepG2 cells Hepatology 52 623 633 20683960 1:CAS:528:DC%2BC3cXhtV2ju7bO
54. H Tang Y Mori 2010 Human herpesvirus-6 entry into host cells Future Microbiol 5 1015 1023 20632802 1:CAS:528:DC%2BC3cXovFersbk%3D
55. 2+ entry Biochim Biophys Acta 1803 1083 1093 20600358 1:CAS:528:DC%2BC3cXptVCktr8%3D
56. S Lin XM Wang PE Nadeau A Mergia 2010 J HIV infection upregulates caveolin 1 expression to restrict virus production Virol 84 9487 9496 1:CAS:528:DC%2BC3cXht1Wgtb7J
57. A Gentil-dit-Maurin S Oun S Almagro S Bouillot M Courçon R Linnepe D Vestweber P Huber E Tillet 2010 Unraveling the distinct distributions of VE- and N-cadherins in endothelial cells: a key role for p120-catenin Exp Cell Res 316 2587 2599 20599949 1:CAS:528:DC%2BC3cXhtVKhtbzP
58. Z Fang N Takizawa KA Wilson TC Smith A Delprato MW Davidson DG Lambright EJ Luna 2010 The membrane-associated protein, supervillin, accelerates F-actin-dependent rapid integrin recycling and cell motility Traffic 11 782 799 20331534 1:CAS:528:DC%2BC3cXms1als7k%3D
59. 2+-ATPase 1 is associated with cholesterol-rich microdomains of human colon adenocarcinoma cells Biochim Biophys Acta 1798 1512 1521 20363212 1:CAS:528:DC%2BC3cXntlalurY%3D
60. K Simons E Ikonen 2000 How cells handle cholesterol Science 290 1721 1726 11099405 1:CAS:528:DC%2BD3cXovVOitbc%3D (Pubitemid 32004797)
61. K Klappe AJ Dijkhuis I Hummel A van Dam PT Ivanova SB Milne DS Myers HA Brown H Permentier JW Kok 2010 Extensive sphingolipid depletion does not affect lipid raft integrity or lipid raft localization and efflux function of the ABC transporter MRP1 Biochem J 430 519 529 20604746 1:CAS:528:DC%2BC3cXhtVyrtb3L
62. T Hayashi TP Su 2010 Cholesterol at the endoplasmic reticulum: roles of the sigma-1 receptor chaperone and implications thereof in human diseases Subcell Biochem 51 381 398 20213551 1:CAS:528:DC%2BC3cXosl2itro%3D
63. M Das DK Das 2009 Lipid raft in cardiac health and disease Curr Cardiol Rev 5 105 111 20436850 1:CAS:528:DC%2BC3cXislOqu7Y%3D
64. M Valapala JK Vishwanatha 2011 Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2 J Biol Chem 286 30911 30925 21737841 1:CAS:528:DC%2BC3MXhtVOktL3I
65. E Feuk-Lagerstedt C Movitz S Pellmé C Dahlgren A Karlsson 2007 Lipid raft proteome of the human neutrophil azurophil granule Proteomics 7 194 205 17152095 1:CAS:528:DC%2BD2sXhslGqtb0%3D (Pubitemid 46184083)
66. V Godoy G Riquelme 2008 Distinct lipid rafts in subdomains from human placental apical syncytiotrophoblast membranes J Membr Biol 224 21 31 18807084 1:CAS:528:DC%2BD1cXht1yqs7rP
67. S Staubach H Razawi FG Hanisch 2009 Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7 Proteomics 9 2820 2835 19415654 1:CAS:528:DC%2BD1MXmtlOmtLw%3D
68. M Golczak A Kirilenko J Bandorowicz-Pikula B Desbat S Pikula 2004 Structure of human annexin A6 at the air-water interface and in a membrane-bound state Biophys J 87 1215 1226 15298924 1:CAS:528:DC%2BD2cXmvFeiurg%3D (Pubitemid 39095098)
69. O Lambert N Cavusoglu J Gallay M Vincent JL Rigaud JP Henry J Ayala-Sanmartin 2004 Novel organization and properties of annexin 2-membrane complexes J Biol Chem 279 10872 10882 14701819 1:CAS:528:DC%2BD2cXitFyitLg%3D (Pubitemid 38401577)
70. M Golczak A Kicinska J Bandorowicz-Pikula R Buchet A Szewczyk S Pikula 2001 Acidic pH-induced folding of annexin VI is a prerequisite for its insertion into lipid bilayers and formation of ion channels by the protein molecules FASEB J 15 1083 1085 11292675 1:CAS:528:DC%2BD3MXivFOrur4%3D
71. R Cornely C Rentero C Enrich T Grewal K Gaus 2011 Annexin A6 is an organizer of membrane microdomains to regulate receptor localization and signalling IUBMB Life 63 1009 1017 21990038 1:CAS:528:DC%2BC3MXhtlOms7nI
72. JY Jeon SY Hwang SH Cho J Choo EK Lee 2010 Effect of cholesterol content on affinity and stability of factor VIII and annexin V binding to a liposomal bilayer membrane Chem Phys Lipids 163 335 340 20132805 1:CAS:528: DC%2BC3cXltFyrtr4%3D
73. PF Almeida A Best A Hinderliter 2011 Monte Carlo simulation of protein-induced lipid demixing in a membrane with interactions derived from experiment Biophys J 101 1930 1937 22004747 1:CAS:528:DC%2BC3MXhtlarsLzE
74. K Kastl M Ross V Gerke C Steinem 2002 Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study Biochemistry 41 10087 10094 12146973 1:CAS:528:DC%2BD38XltFOjsL0%3D (Pubitemid 34839754)
75. S Heyraud M Jaquinod C Durmort E Dambroise E Concord JP Schaal P Huber D Gulino-Debrac 2008 Contribution of annexin 2 to the architecture of mature endothelial adherens junctions Mol Cell Biol 28 1657 1668 18160703 1:CAS:528:DC%2BD1cXivVajtL8%3D
76. J Ayala-Sanmartin 2001 Cholesterol enhances phospholipid binding and aggregation of annexins by their core domain Biochem Biophys Res Commun 283 72 79 11322769 (Pubitemid 32912538)
77. S Chasserot-Golaz N Vitale E Umbrecht-Jenck D Knight V Gerke MF Bader 2005 Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles Mol Biol Cell 16 1108 1119 15635098 1:CAS:528:DC%2BD2MXit1SrsbY%3D (Pubitemid 40349549)
78. I de Diego F Schwartz H Siegfried P Dauterstedt J Heeren U Beisiegel C Enrich T Thomas Grewal 2002 Cholesterol modulates the membrane binding and intracellular distribution of annexin 6 J Biol Chem 277 32187 32194 12070178 (Pubitemid 34969033)
79. 2+ concentration Biochim Biophys Acta 1510 18 28 11342144 (Pubitemid 32149882)
80. E Morel R Parton J Gruenberg 2009 Annexin A2-dependent polymerization of actin mediates endosome biogenesis Dev Cell 16 445 457 19289089 1:CAS:528:DC%2BD1MXjs1ynsrg%3D
81. S Jäckle U Beisiegel F Rinninger F Buck A Grigoleit A Block I Gröger H Greten E Windler 1994 Annexin VI, a marker protein of hepatocytic endosomes J Biol Chem 269 1026 1032 7904597 (Pubitemid 24032480)
82. A Pol D Ortega C Enrich 1997 Identification of cytoskeleton-associated proteins in isolated rat liver endosomes Biochem J 327 741 746 9581551 1:CAS:528:DyaK2sXns1alsro%3D (Pubitemid 27487680)
83. T Grewal J Heeren D Mewawala T Schnitgerhans D Wendt G Salomon C Enrich U Beisiegel S Jäckle 2000 Annexin VI stimulates endocytosis and is involved in the trafficking of low density lipoprotein to the prelysosomal compartment J Biol Chem 275 33806 33813 10940299 1:CAS:528:DC%2BD3cXnvVyjtrY%3D
84. M Reverter C Rentero SV de Muga A Alvarez-Guaita V Mulay R Cairns P Wood K Monastyrskaya A Pol F Tebar J Blasi T Grewal C Enrich 2011 Cholesterol transport from late endosomes to the Golgi regulates t-SNARE trafficking, assembly, and function Mol Biol Cell 22 4108 4123 22039070 1:CAS:528: DC%2BC3MXhsV2qu7bO
85. M Pons G Ihrke S Koch M Biermer A Pol T Grewal S Jäckle C Enrich 2000 Late endocytic compartments are major sites of annexin VI localization in NRK fibroblasts and polarized WIF-B hepatoma cells Exp Cell Res 257 33 47 10854052 1:CAS:528:DC%2BD3cXjvFCrsr4%3D (Pubitemid 30324642)
86. M Pons T Grewal E Rius T Schnitgerhans S Jäckle C Enrich 2001 Evidence for the involvement of annexin 6 in the trafficking between the endocytic compartment and lysosomes Exp Cell Res 269 13 22 11525635 1:CAS:528:DC%2BD3MXmt1Kgu7g%3D (Pubitemid 32848485)
87. T Grewal C Enrich 2009 Annexins - modulators of EGF receptor signalling and trafficking Cell Signal 21 847 858 19385045 1:CAS:528:DC%2BD1MXjslKkt7c%3D
88. EB Babiychuk RJTS Palstra J Schaller U Kämpfer A Draeger 1999 Annexin VI participates in the formation of a reversible, membrane-cytoskeleton complex in smooth muscle cells J Biol Chem 274 35191 35195 10575003 1:CAS:528:DyaK1MXnvFyrurw%3D (Pubitemid 129509576)
89. MJ Hayes U Rescher V Gerke SE Moss 2004 Annexin-actin interactions Traffic 5 571 576 15260827 1:CAS:528:DC%2BD2cXms1ektrs%3D (Pubitemid 39144487)
90. 2+ entry by stabilizing the cortical actin cytoskeleton J Biol Chem 284 17227 17242 19386597 1:CAS:528:DC%2BD1MXntFCjtb8%3D
91. T Grewal C Enrich 2006 Molecular mechanisms involved in Ras inactivation: the annexin A6-p120GAP complex BioEssays 28 1211 1220 17120209 1:CAS:528:DC%2BD2sXislGjtQ%3D%3D (Pubitemid 44925441)
92. F Lafont S Lecat P Verkade K Simons 1998 Annexin XIIIb associates with lipid microdomains to function in apical delivery J Cell Biol 142 1413 1427 9744874 1:CAS:528:DyaK1cXmt1anur8%3D (Pubitemid 28452593)
93. K Astanina CI Delebinski D Delacour R Jacob 2010 Annexin XIIIb guides raft-dependent and -independent apical traffic in MDCK cells Eur J Cell Biol 89 799 806 20708818 1:CAS:528:DC%2BC3cXhtFGjs7jM
94. S Faiss K Kastl A Janshoff C Steinem 2008 Formation of irreversibly bound annexin A1 protein domains on POPC/POPS solid supported membranes Biochem Biophys Acta 1778 1601 1610 18237543 1:CAS:528:DC%2BD1cXnsFCrsLc%3D
95. N Mayran RG Parton J Gruenberg 2003 Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells EMBO J 22 3242 3253 12839987 1:CAS:528:DC%2BD3sXltFyht7c%3D (Pubitemid 36834855)
96. M Ross V Gerke C Steinem 2003 Membrane composition affects the reversibility of annexin A2t binding to solid supported membranes: a QCM study Biochemistry 42 3131 3141 12627981 1:CAS:528:DC%2BD3sXht1eltro%3D (Pubitemid 36331559)
97. D Zeuschner W Stoorvogel V Gerke 2001 Association of annexin 2 with recycling endosomes requires either calcium- or cholesterol-stabilized membrane domains Eur J Cell Biol 80 499 507 11561901 1:CAS:528:DC%2BD3MXns1KitL0%3D (Pubitemid 32821621)
98. JY Jeon SY Hwang SH Cho J Choo EK Lee 2010 Effect of cholesterol content on affinity and stability of factor VIII and annexin V binding to a liposomal bilayer membrane Chem Phys Lipids 163 335 340 20132805 1:CAS:528: DC%2BC3cXltFyrtr4%3D
99. PF Almeida A Best A Hinderliter 2011 Monte Carlo simulation of protein-induced lipid demixing in a membrane with interactions derived from experiment Biophys J 101 1930 1937 22004747 1:CAS:528:DC%2BC3MXhtlarsLzE
100. SA Johnson BM Stinson MS Go LM Carmona JI Reminick X Fang T Baumgart 2010 Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles Biochim Biophys Acta 1798 1427 1435 20230780 1:CAS:528:DC%2BC3cXntVejsb4%3D
101. M Domon G Matar A Strzelecka-Kiliszek J Bandorowicz-Pikula S Pikula F Besson 2010 Interaction of annexin A6 with cholesterol rich membranes is pH-dependent and mediated by the sterol OH J Colloid Interface Sci 346 436 441 20363475 1:CAS:528:DC%2BC3cXlsVemu7w%3D
102. X Li KA Becker Y Zhang 2010 Ceramide in redox signaling and cardiovascular diseases Cell Physiol Biochem. 26 41 48 20502003
103. S Schwarzer M Nobles A Tinker 2010 Do caveolae have a role in the fidelity and dynamics of receptor activation of G-protein-gated inwardly rectifying potassium channels? J Biol Chem 285 27817 27826 20562107 1:CAS:528:DC%2BC3cXhtVOnsL3N
104. T Tobe 2010 Cytoskeleton-modulating effectors of enteropathogenic and enterohemorrhagic Escherichia coli: role of EspL2 in adherence and an alternative pathway for modulating cytoskeleton through annexin A2 function FEBS J 277 2403 2408 20477868 1:CAS:528:DC%2BC3cXmvFCgs7Y%3D
105. A Ono 2010 Relationships between plasma membrane microdomains and HIV-1 assembly Biol Cell 102 335 350 20356318 1:CAS:528:DC%2BC3cXktFyntLk%3D
106. KS Vetrivel G Thinakaran 2010 Membrane rafts in Alzheimer's disease beta-amyloid production Biochim Biophys Acta 1801 860 867 20303415 1:CAS:528:DC%2BC3cXntlags70%3D
107. CL Schengrund 2010 Lipid rafts: keys to neurodegeneration Brain Res Bull 82 7 17 20206240 1:CAS:528:DC%2BC3cXlsFaju7g%3D
108. KM Boini C Zhang M Xia WQ Han C Brimson JL Poklis PL Li 2010 Visfatin-induced lipid raft redox signaling platforms and dysfunction in glomerular endothelial cells Biochim Biophys Acta 1801 1294 1304 20858552 1:CAS:528:DC%2BC3cXhtlShtLzK
109. T Murai Y Maruyama K Mio H Nishiyama M Suga C Sato 2011 Low cholesterol triggers membrane microdomain-dependent CD44 shedding and suppresses tumor cell migration J Biol Chem 286 1999 2007 21087933 1:CAS:528:DC%2BC3MXlsFSrsQ%3D%3D
110. EK Park EJ Lee SH Lee KH Koo JY Sung EH Hwang JH Park CW Kim KC Jeong BK Park YN Kim 2010 Induction of apoptosis by the ginsenoside Rh2 by internalization of lipid rafts and caveolae and inactivation of Akt Br J Pharmacol 160 1212 1223 20590613 1:CAS:528:DC%2BC3cXpsFGjt7g%3D
111. S Staubach FG Hanisch 2011 Lipid rafts: signaling and sorting platforms of cells and their roles in cancer Expert Rev Proteomics 8 263 277 21501018 1:CAS:528:DC%2BC3MXkvF2ht7Y%3D
112. N Assaife-Lopes VC Sousa DB Pereira JA Ribeiro MV Chao AM Sebastião 2010 Activation of adenosine A2A receptors induces TrkB translocation and increases BDNF-mediated phospho-TrkB localization in lipid rafts: implications for neuromodulation J Neurosci 30 8468 8480 20573894 1:CAS:528: DC%2BC3cXos1Kntbo%3D
113. GR Chichili AD Westmuckett W Rodgers 2010 T cell signal regulation by the actin cytoskeleton J Biol Chem 285 14737 14746 20194498 1:CAS:528: DC%2BC3cXlsVOhsbg%3D
114. J Ponce D Brea M Carrascal V Guirao N Degregorio-Rocasolano T Sobrino J Castillo A Dávalos T Gasull 2010 The effect of simvastatin on the proteome of detergent-resistant membrane domains: decreases of specific proteins previously related to cytoskeleton regulation, calcium homeostasis and cell fate Proteomics 10 1954 1965 20217863 1:CAS:528:DC%2BC3cXmtVylurg%3D
115. MP Carrasco JM Jiménez-López P Ríos-Marco JL Segovia C Marco 2010 Disruption of cellular cholesterol transport and homeostasis as a novel mechanism of action of membrane-targeted alkylphospholipid analogues Br J Pharmacol 160 355 366 20423345 1:CAS:528:DC%2BC3cXpslyqsLg%3D
116. AJ Pommier G Alves E Viennois S Bernard Y Communal B Sion G Marceau C Damon K Mouzat F Caira S Baron JM Lobaccaro 2010 Liver X Receptor activation downregulates AKT survival signaling in lipid rafts and induces apoptosis of prostate cancer cells Oncogene 29 2712 2723 20190811 1:CAS:528: DC%2BC3cXisFOktbs%3D
117. M Fuller 2010 Sphingolipids: the nexus between Gaucher disease and insulin resistance Lipids Health Dis 9 113 20937139
118. X Li KA Becker Y Zhang 2010 Ceramide in redox signaling and cardiovascular diseases Cell Physiol Biochem 26 41 48 20502003
119. F Stögbauer J Weigert M Neumeier J Wanninger D Sporrer M Weber A Schefler C Enrich P Wood T Grewal C Aslanidis C Buechler 2009 Annexin A6 is highly abundant in monocytes of obese and type 2 diabetic individuals and is downregulated by adiponectin in vitro Exp Mol Med 41 501 507 19322030
120. ME Sztolsztener A Strzelecka-Kiliszek S Pikula A Tylki-Szymanska J Bandorowicz-Pikula 2009 Cholesterol as a factor regulating intracellular localization of annexin A6 in Niemann-Pick type C human skin fibroblasts Arch Biochem Biophys 493 221 233 19900398
121. 2+-dependent manner Biochem Biophys Res Commun 405 192 196 21216236 1:CAS:528:DC%2BC3MXhvFKmt7k%3D
122. R Schiffmann 2010 Therapeutic approaches for neuronopathic lysosomal storage disorders J Inherit Metab Dis 33 373 379 20162366 1:CAS:528: DC%2BC3cXoslyntbw%3D
123. C Scott YA Ioannou 2004 The NPC1 protein: structure implies function Biochim Biophys Acta 1685 8 13 15465421 1:CAS:528:DC%2BD2cXotFCksbo%3D (Pubitemid 39311806)
124. TS Blom MD Linder K Snow H Pihko MW Hess E Jokitalo V Veckman AC Syvänen E Ikonen 2003 Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann-Pick type C disease Hum Mol Genet 12 257 272 12554680 1:CAS:528:DC%2BD3sXitVWqtrg%3D (Pubitemid 36204423)
125. DS Ory 2000 Niemann-Pick type C: a disorder of cellular cholesterol trafficking Biochim Biophys Acta 1529 331 339 11111100 1:CAS:528: DC%2BD3cXosFCgtr8%3D
126. DC Ko J Binkley A Sidow MP Scott 2003 The integrity of a cholesterol-binding pocket in Niemann-Pick C2 protein is necessary to control lysosome cholesterol levels Proc Natl Acad Sci USA 100 2518 2525 12591949 1:CAS:528:DC%2BD3sXitVais7g%3D (Pubitemid 36297531)
127. RE Infante ML Wang A Radhakrishnan HJ Kwon MS Brown JL Goldstein 2008 NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes Proc Natl Acad Sci USA 105 15287 15292 18772377 1:CAS:528:DC%2BD1cXht1GntrfK
128. S Mukherjee F Maxfield 2000 Role of membrane organization and membrane domains in endocytic lipid trafficking Traffic 1 203 211 11208103 1:CAS:528:DC%2BD3cXktl2msLg%3D
129. MT Vanier G Millat 2003 Niemann-Pick disease type C Clin Genet 64 269 281 12974729 1:STN:280:DC%2BD3svos1ektw%3D%3D (Pubitemid 37236127)
130. TY Chang PC Reid S Sugii N Ohgami JC Cruz CC Chang 2005 Niemann-Pick type C disease and intracellular cholesterol trafficking J Biol Chem 280 20917 20920 15831488 1:CAS:528:DC%2BD2MXks1emtbY%3D (Pubitemid 40805646)
131. Y Lange J Ye M Rigney TL Steck 1999 Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol J Lipid Res 40 2264 2270 10588952 1:CAS:528:DC%2BD3cXitV2l (Pubitemid 30017528)
132. GM Troup SP Wrenn 2004 Temperature and cholesterol composition-dependent behavior of 1-myristoyl-2-[12-[(5-dimethylamino-1-naphthalenesulfonyl) amino] dodecanoyl]-sn-glycero-3-phosphocholine in 1, 2-dimyristoyl-sn-glycero-3- phosphocholine membranes Chem Phys Lipids 131 167 182 15351269 1:CAS:528:DC%2BD2cXntlSnt7o%3D (Pubitemid 39207456)
133. Cornely R, Rentero C, Enrich C, Grewal T, Gaus K (2011) Annexin A6 is an organizer of membrane microdomains to regulate receptor localization and signalling. IUBMB Life 63:1009-1017
134. D te Vruchte E Lloyd-Evans RJ Veldman DC Neville RA Dwek FM Platt WJ van Blitterswijk DJ Sillence 2004 Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport J Biol Chem 279 26167 26175 15078881 1:CAS:528:DC%2BD2cXkvVWgsr8%3D (Pubitemid 38798762)
135. L Cubells S Vilà de Muga F Tebar P Wood R Evans M Ingelmo-Torres M Calvo K Gaus A Pol T Grewal C Enrich 2007 Annexin A6-induced alterations in cholesterol transport and caveolin export from the Golgi complex Traffic 8 1568 1589 17822395 1:CAS:528:DC%2BD2sXht1ynsrzM (Pubitemid 47578362)
136. L Cubells S Vilà de Muga F Tebar JV Bonventre J Balsinde A Pol T Grewal C Enrich 2008 Annexin A6-induced inhibition of cytoplasmic phospholipase A2 is linked to caveolin-1 export from the Golgi J Biol Chem 283 10174 10183 18245088 1:CAS:528:DC%2BD1cXkt1alu7c%3D
137. G Mayer S Poirier NG Seidah 2008 Annexin A2 is a C-terminal PCSK9-binding protein that regulates endogenous low density lipoprotein receptor levels J Biol Chem 283 31791 31801 18799458 1:CAS:528:DC%2BD1cXhtlCjsbvK
138. J Davignon G Dubuc NG Seidah 2010 The influence of PCSK9 polymorphisms on serum low-density lipoprotein cholesterol and risk of atherosclerosis Curr Atheroscler Rep 12 308 315 20623344 1:CAS:528:DC%2BC3cXhtlyqurfJ
139. MA Valasek J Weng PW Shaul RG Anderson JJ Repa 2005 Caveolin-1 is not required for murine intestinal cholesterol transport J Biol Chem 280 28103 28109 15919660 1:CAS:528:DC%2BD2MXmsV2jsrk%3D (Pubitemid 41076928)