Skip to main content

Advertisement

SpringerLink
Log in

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

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Growing evidence suggests that membrane microdomains enriched in cholesterol and sphingomyelin are sites for numerous cellular processes, including signaling, vesicular transport, interaction with pathogens, and viral infection, etc. Recently some members of the annexin family of conserved calcium and membrane-binding proteins have been recognized as cholesterol-interacting molecules and suggested to play a role in the formation, stabilization, and dynamics of membrane microdomains to affect membrane lateral organization and to attract other proteins and signaling molecules onto their territory. Furthermore, annexins were implicated in the interactions between cytosolic and membrane molecules, in the turnover and storage of cholesterol and in various signaling pathways. In this review, we focus on the mechanisms of interaction of annexins with lipid microdomains and the role of annexins in membrane microdomains dynamics including possible participation of the domain-associated forms of annexins in the etiology of human lysosomal storage disease called Niemann-Pick type C disease, related to the abnormal storage of cholesterol in the lysosome-like intracellular compartment. The involvement of annexins and cholesterol/sphingomyelin-enriched membrane microdomains in other pathologies including cardiac dysfunctions, neurodegenerative diseases, obesity, diabetes mellitus, and cancer is likely, but is not supported by substantial experimental observations, and therefore awaits further clarification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Ramjiawan B, Czubryt MP, Gilchrist JS, Pierce GN (1996) Nuclear membrane cholesterol can modulate nuclear nucleoside triphosphatase activity. J Cell Biochem 63:442–452

    PubMed  CAS  Google Scholar 

  2. Reineri S, Bertoni A, Sanna E, Baldassarri S, Sarasso C, Zanfa M, Canobbio I, Torti M, Sinigaglia F (2007) Membrane lipid rafts coordinate estrogen-dependent signaling in human platelets. Biochim Biophys Acta 1773:273–278

    PubMed  CAS  Google Scholar 

  3. Batetta B, Sanna F (2006) Cholesterol metabolism during cell growth: which role for the plasma membrane? Eur J Lipid Sci Technol 108:687–699

    CAS  Google Scholar 

  4. Liu JP, Tang Y, Zhou S, Toh BH, McLean C, Li H (2010) Cholesterol involvement in the pathogenesis of neurodegenerative diseases. Mol Cell Neurosci 43:33–42

    PubMed  CAS  Google Scholar 

  5. Grewal T, Koese M, Rentero C, Enrich C (2010) Annexin A6-regulator of the EGFR/Ras signalling pathway and cholesterol homeostasis. Int J Biochem Cell Biol 42:580–584

    PubMed  CAS  Google Scholar 

  6. Enrich C, Rentero C, de Muga SV, Reverter M, Mulay V, Wood P, Koese M, Grewal T (2011) Annexin A6-Linking Ca2+ signaling with cholesterol transport. Biochim Biophys Acta 1813:935–947

    PubMed  CAS  Google Scholar 

  7. Harder T, Kellner R, Parton RG, Gruenberg J (1997) Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol Biol Cell 8:533–545

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  9. Babiychuk EB, Draeger A (2000) Annexins in cell membrane dynamics. Ca2+–regulated association of lipid microdomains. J Cell Biol 150:1113–1124

    PubMed  CAS  Google Scholar 

  10. Babiychuk EB, Draeger A (2006) Biochemical characterization of detergent-resistant membranes: a systematic approach. Biochem J 397:407–416

    PubMed  CAS  Google Scholar 

  11. Carafoli E (2010) The fateful encounter of mitochondria with calcium: how did it happen? Biochim Biophys Acta 1797:595–606

    PubMed  CAS  Google Scholar 

  12. Haiech J, Audran E, Fève M, Ranjeva R, Kilhoffer MC (2011) Revisiting intracellular calcium signaling semantics. Biochimie 93:2029–2037

    Google Scholar 

  13. Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Natl Rev Mol Cell Biol 6:449–461

    CAS  Google Scholar 

  14. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Natl Rev Mol Cell Biol 9:99–111

    CAS  Google Scholar 

  15. Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371

    PubMed  CAS  Google Scholar 

  16. Draeger A, Monastyrskaya K, Babiychuk EB (2011) Plasma membrane repair and cellular damage control: the annexin survival kit. Biochem Pharmcol 81:703–712

    CAS  Google Scholar 

  17. Futter CE, White IJ (2007) Annexins and endocytosis. Traffic 8:951–958

    PubMed  CAS  Google Scholar 

  18. Hayes MJ, Longbottom RE, Evans MA, Moss SE (2007) Annexinopathies. Subcell Biochem 45:1–28

    PubMed  CAS  Google Scholar 

  19. Lim LH, Pervaiz S (2007) Annexin 1: the new face of an old molecule. FASEB J 21:968–975

    PubMed  CAS  Google Scholar 

  20. Fatimathas L, Moss SE (2010) Annexins as disease modifiers. Histol Histopathol 25:527–532

    PubMed  CAS  Google Scholar 

  21. Mukherjee S, Maxfield FR (2004) Lipid and cholesterol trafficking in NPC. Biochim Biophys Acta 1685:28–37

    PubMed  CAS  Google Scholar 

  22. Lindner R, Naim HY (2009) Domains in biological membranes. Exp Cell Res 315:2871–2878

    PubMed  CAS  Google Scholar 

  23. Pike LJ (2009) The challenge of lipid rafts. J Lipid Res. 50 Suppl:S323-S328

  24. Hao YH, Chen JW (2001) Influence of cholesterol on the biophysical properties of the sphingomyelin/DOPC binary system. J Membr Biol 183:85–92

    PubMed  CAS  Google Scholar 

  25. Schuck S, Simons K (2004) Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J Cell Sci 117:5955–5964

    PubMed  CAS  Google Scholar 

  26. Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3:a004697

    PubMed  CAS  Google Scholar 

  27. Bonnin S, El Kirat K, Becchi M, Dubois M, Grangeasse C, Giraud C, Prigent A-F, Lagarde M, Roux B, Besson F (2003) Protein and lipid analysis of detergent-resistant membranes isolated from bovine kidney. Biochimie 85:1237–1244

    PubMed  CAS  Google Scholar 

  28. Coskun U, Simons K (2010) Membrane rafting: from apical sorting to phase segregation. FEBS Lett 584:1685–1693

    PubMed  CAS  Google Scholar 

  29. Maeda Y, Kinoshita T (2011) Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins. Prog Lipid Res 50:411–424

    PubMed  CAS  Google Scholar 

  30. Giocondi MC, Besson F, Dosset P, Milhiet PE, Le Grimellec C (2007) Remodeling of ordered membrane domains by GPI-anchored intestinal alkaline phosphatase. Langmuir 23:9358–9364

    PubMed  CAS  Google Scholar 

  31. Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49:6305–6316

    PubMed  CAS  Google Scholar 

  32. Coskun U, Simons K (2011) Cell membranes: the lipid perspective. Structure 19:1543–1548

    Google Scholar 

  33. Edidin M (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32:257–283

    PubMed  CAS  Google Scholar 

  34. Shaikh SR, Edidin MA (2006) Membranes are not just rafts. Chem Phys Lipids 144:1–3

    PubMed  CAS  Google Scholar 

  35. Shah MB, Sehgal PB (2007) Nondetergent isolation of rafts. Methods Mol Biol 398:21–28

    PubMed  CAS  Google Scholar 

  36. Persaud-Sawin DA, Lightcap S, Harry GJ (2009) Isolation of rafts from mouse brain tissue by a detergent-free method. J Lipid Res 50:759–767

    PubMed  CAS  Google Scholar 

  37. Wassall SR, Brzustowicz MR, Shaikh SR, Cherezov V, Caffrey M, Stillwell W (2004) Order from disorder, corralling cholesterol with chaotic lipids. The role of polyunsaturated lipids in membrane raft formation. Chem Phys Lipids 132:79–88

    PubMed  CAS  Google Scholar 

  38. Castro BM, Silva LC, Fedorov A, de Almeida RF, Prieto M (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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  40. Quinn PJ, Wolf C (2010) An X-ray diffraction study of model membrane raft structures. FEBS J 277:4685–4698

    PubMed  CAS  Google Scholar 

  41. Martinez-Seara H, Róg T, Karttunen M, Vattulainen I, Reigada R (2010) Cholesterol induces specific spatial and orientational order in cholesterol/phospholipid membranes. PLoS One 5:e11162

    PubMed  Google Scholar 

  42. Nasir MN, Besson F (2011) Specific interactions of mycosubtilin with cholesterol-containing artificial membranes. Langmuir 27:10785–10792

    PubMed  CAS  Google Scholar 

  43. Björkbom A, Róg T, Kaszuba K, Kurita M, Yamaguchi S, Lönnfors M, Nyholm TK, Vattulainen I, Katsumura S, Slotte JP (2010) Effect of sphingomyelin headgroup size on molecular properties and interactions with cholesterol. Biophys J 99:3300–3308

    PubMed  Google Scholar 

  44. Kahya N (2010) Protein-protein and protein-lipid interactions in domain-assembly: lessons from giant unilamellar vesicles. Biochim Biophys Acta 1798:1392–1398

    PubMed  CAS  Google Scholar 

  45. Banerji S, Ngo M, Lane CF, Robinson CA, Minogue S, Ridgway ND (2010) Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the Golgi apparatus requires phosphatidylinositol 4-kinase IIα. Mol Biol Cell 21:4141–4150

    PubMed  CAS  Google Scholar 

  46. Bonnon C, Wendeler MW, Paccaud JP, Hauri HP (2010) Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J Cell Sci 123:1705–1715

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  48. Lasley RD (2011) Adenosine receptors and membrane microdomains. Biochim Biophys Acta 1808:1284–1289

    PubMed  CAS  Google Scholar 

  49. Zhang C, Li PL (2010) Membrane raft redox signalosomes in endothelial cells. Free Radic Res 44:831–842

    PubMed  CAS  Google Scholar 

  50. Dart C (2010) Lipid microdomains and the regulation of ion channel function. J Physiol 588:3169–3178

    PubMed  CAS  Google Scholar 

  51. Ganapathi SB, Fox TE, Kester M, Elmslie KS (2010) Ceramide modulates HERG potassium channel gating by translocation into lipid rafts. Am J Physiol Cell Physiol 299:C74–C86

    PubMed  CAS  Google Scholar 

  52. Sones WR, Davis AJ, Leblanc N, Greenwood IA (2010) Cholesterol depletion alters amplitude and pharmacology of vascular calcium-activated chloride channels. Cardiovasc Res 87:476–484

    PubMed  CAS  Google Scholar 

  53. Woudenberg J, Rembacz KP, Hoekstra M, Pellicoro A, van den Heuvel FA, Heegsma J, van Ijzendoorn SC, Holzinger A, Imanaka T, Moshage H, Faber KN (2010) Lipid rafts are essential for peroxisome biogenesis in HepG2 cells. Hepatology 52:623–633

    PubMed  CAS  Google Scholar 

  54. Tang H, Mori Y (2010) Human herpesvirus-6 entry into host cells. Future Microbiol 5:1015–1023

    PubMed  CAS  Google Scholar 

  55. Galan C, Woodard GE, Dionisio N, Salido GM, Rosado JA (2010) Lipid rafts modulate the activation but not the maintenance of store-operated Ca2+ entry. Biochim Biophys Acta 1803:1083–1093

    PubMed  CAS  Google Scholar 

  56. Lin S, Wang XM, Nadeau PE, Mergia A (2010) J HIV infection upregulates caveolin 1 expression to restrict virus production. Virol 84:9487–9496

    CAS  Google Scholar 

  57. Gentil-dit-Maurin A, Oun S, Almagro S, Bouillot S, Courçon M, Linnepe R, Vestweber D, Huber P, Tillet E (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

    PubMed  CAS  Google Scholar 

  58. Fang Z, Takizawa N, Wilson KA, Smith TC, Delprato A, Davidson MW, Lambright DG, Luna EJ (2010) The membrane-associated protein, supervillin, accelerates F-actin-dependent rapid integrin recycling and cell motility. Traffic 11:782–799

    PubMed  CAS  Google Scholar 

  59. Baron S, Vangheluwe P, Sepúlveda MR, Wuytack F, Raeymaekers L, Vanoevelen J (2010) The secretory pathway Ca2+-ATPase 1 is associated with cholesterol-rich microdomains of human colon adenocarcinoma cells. Biochim Biophys Acta 1798:1512–1521

    PubMed  CAS  Google Scholar 

  60. Simons K, Ikonen E (2000) How cells handle cholesterol. Science 290:1721–1726

    PubMed  CAS  Google Scholar 

  61. Klappe K, Dijkhuis AJ, Hummel I, van Dam A, Ivanova PT, Milne SB, Myers DS, Brown HA, Permentier H, Kok JW (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

    PubMed  CAS  Google Scholar 

  62. Hayashi T, Su TP (2010) Cholesterol at the endoplasmic reticulum: roles of the sigma-1 receptor chaperone and implications thereof in human diseases. Subcell Biochem 51:381–398

    PubMed  CAS  Google Scholar 

  63. Das M, Das DK (2009) Lipid raft in cardiac health and disease. Curr Cardiol Rev 5:105–111

    PubMed  CAS  Google Scholar 

  64. Valapala M, Vishwanatha JK (2011) Lipid raft endocytosis and exosomal transport facilitate extracellular trafficking of annexin A2. J Biol Chem 286:30911–30925

    PubMed  CAS  Google Scholar 

  65. Feuk-Lagerstedt E, Movitz C, Pellmé S, Dahlgren C, Karlsson A (2007) Lipid raft proteome of the human neutrophil azurophil granule. Proteomics 7:194–205

    PubMed  CAS  Google Scholar 

  66. Godoy V, Riquelme G (2008) Distinct lipid rafts in subdomains from human placental apical syncytiotrophoblast membranes. J Membr Biol 224:21–31

    PubMed  CAS  Google Scholar 

  67. Staubach S, Razawi H, Hanisch FG (2009) Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9:2820–2835

    PubMed  CAS  Google Scholar 

  68. Golczak M, Kirilenko A, Bandorowicz–Pikula J, Desbat B, Pikula S (2004) Structure of human annexin A6 at the air–water interface and in a membrane–bound state. Biophys J 87:1215–1226

    PubMed  CAS  Google Scholar 

  69. Lambert O, Cavusoglu N, Gallay J, Vincent M, Rigaud JL, Henry JP, Ayala–Sanmartin J (2004) Novel organization and properties of annexin 2–membrane complexes. J Biol Chem 279:10872–10882

    PubMed  CAS  Google Scholar 

  70. Golczak M, Kicinska A, Bandorowicz-Pikula J, Buchet R, Szewczyk A, Pikula S (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

    PubMed  CAS  Google Scholar 

  71. 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

    PubMed  CAS  Google Scholar 

  72. Jeon JY, Hwang SY, Cho SH, Choo J, Lee EK (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

    PubMed  CAS  Google Scholar 

  73. Almeida PF, Best A, Hinderliter A (2011) Monte Carlo simulation of protein-induced lipid demixing in a membrane with interactions derived from experiment. Biophys J 101:1930–1937

    PubMed  CAS  Google Scholar 

  74. Kastl K, Ross M, Gerke V, Steinem C (2002) Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study. Biochemistry 41:10087–10094

    PubMed  CAS  Google Scholar 

  75. Heyraud S, Jaquinod M, Durmort C, Dambroise E, Concord E, Schaal JP, Huber P, Gulino-Debrac D (2008) Contribution of annexin 2 to the architecture of mature endothelial adherens junctions. Mol Cell Biol 28:1657–1668

    PubMed  CAS  Google Scholar 

  76. Ayala–Sanmartin J (2001) Cholesterol enhances phospholipid binding and aggregation of annexins by their core domain. Biochem Biophys Res Commun 283:72–79

    PubMed  Google Scholar 

  77. Chasserot-Golaz S, Vitale N, Umbrecht-Jenck E, Knight D, Gerke V, Bader MF (2005) Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol Biol Cell 16:1108–1119

    PubMed  CAS  Google Scholar 

  78. de Diego I, Schwartz F, Siegfried H, Dauterstedt P, Heeren J, Beisiegel U, Enrich C, Thomas Grewal T (2002) Cholesterol modulates the membrane binding and intracellular distribution of annexin 6. J Biol Chem 277:32187–32194

    PubMed  Google Scholar 

  79. Ayala–Sanmartin J, Henry JP, Pradel LA (2001) Cholesterol regulates membrane binding and aggregation by annexin 2 at submicromolar Ca2+ concentration. Biochim Biophys Acta 1510:18–28

    PubMed  Google Scholar 

  80. Morel E, Parton R, Gruenberg J (2009) Annexin A2–dependent polymerization of actin mediates endosome biogenesis. Dev Cell 16:445–457

    PubMed  CAS  Google Scholar 

  81. Jäckle S, Beisiegel U, Rinninger F, Buck F, Grigoleit A, Block A, Gröger I, Greten H, Windler E (1994) Annexin VI, a marker protein of hepatocytic endosomes. J Biol Chem 269:1026–1032

    PubMed  Google Scholar 

  82. Pol A, Ortega D, Enrich C (1997) Identification of cytoskeleton–associated proteins in isolated rat liver endosomes. Biochem J 327:741–746

    PubMed  CAS  Google Scholar 

  83. Grewal T, Heeren J, Mewawala D, Schnitgerhans T, Wendt D, Salomon G, Enrich C, Beisiegel U, Jäckle S (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

    PubMed  CAS  Google Scholar 

  84. Reverter M, Rentero C, de Muga SV, Alvarez-Guaita A, Mulay V, Cairns R, Wood P, Monastyrskaya K, Pol A, Tebar F, Blasi J, Grewal T, Enrich C (2011) Cholesterol transport from late endosomes to the Golgi regulates t-SNARE trafficking, assembly, and function. Mol Biol Cell 22:4108–4123

    PubMed  CAS  Google Scholar 

  85. Pons M, Ihrke G, Koch S, Biermer M, Pol A, Grewal T, Jäckle S, Enrich C (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

    PubMed  CAS  Google Scholar 

  86. Pons M, Grewal T, Rius E, Schnitgerhans T, Jäckle S, Enrich C (2001) Evidence for the involvement of annexin 6 in the trafficking between the endocytic compartment and lysosomes. Exp Cell Res 269:13–22

    PubMed  CAS  Google Scholar 

  87. Grewal T, Enrich C (2009) Annexins - modulators of EGF receptor signalling and trafficking. Cell Signal 21:847–858

    PubMed  CAS  Google Scholar 

  88. Babiychuk EB, Palstra RJTS, Schaller J, Kämpfer U, Draeger A (1999) Annexin VI participates in the formation of a reversible, membrane–cytoskeleton complex in smooth muscle cells. J Biol Chem 274:35191–35195

    PubMed  CAS  Google Scholar 

  89. Hayes MJ, Rescher U, Gerke V, Moss SE (2004) Annexin–actin interactions. Traffic 5:571–576

    PubMed  CAS  Google Scholar 

  90. Monastyrskaya K, Babiychuk EB, Hostettler A, Wood P, Grewal T, Draeger A (2009) Plasma membrane-associated annexin A6 reduces Ca2+ entry by stabilizing the cortical actin cytoskeleton. J Biol Chem 284:17227–17242

    PubMed  CAS  Google Scholar 

  91. Grewal T, Enrich C (2006) Molecular mechanisms involved in Ras inactivation: the annexin A6–p120GAP complex. BioEssays 28:1211–1220

    PubMed  CAS  Google Scholar 

  92. Lafont F, Lecat S, Verkade P, Simons K (1998) Annexin XIIIb associates with lipid microdomains to function in apical delivery. J Cell Biol 142:1413–1427

    PubMed  CAS  Google Scholar 

  93. Astanina K, Delebinski CI, Delacour D, Jacob R (2010) Annexin XIIIb guides raft-dependent and -independent apical traffic in MDCK cells. Eur J Cell Biol 89:799–806

    PubMed  CAS  Google Scholar 

  94. Faiss S, Kastl K, Janshoff A, Steinem C (2008) Formation of irreversibly bound annexin A1 protein domains on POPC/POPS solid supported membranes. Biochem Biophys Acta 1778:1601–1610

    PubMed  CAS  Google Scholar 

  95. Mayran N, Parton RG, Gruenberg J (2003) Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J 22:3242–3253

    PubMed  CAS  Google Scholar 

  96. Ross M, Gerke V, Steinem C (2003) Membrane composition affects the reversibility of annexin A2t binding to solid supported membranes: a QCM study. Biochemistry 42:3131–3141

    PubMed  CAS  Google Scholar 

  97. Zeuschner D, Stoorvogel W, Gerke V (2001) Association of annexin 2 with recycling endosomes requires either calcium- or cholesterol-stabilized membrane domains. Eur J Cell Biol 80:499–507

    PubMed  CAS  Google Scholar 

  98. Jeon JY, Hwang SY, Cho SH, Choo J, Lee EK (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

    PubMed  CAS  Google Scholar 

  99. Almeida PF, Best A, Hinderliter A (2011) Monte Carlo simulation of protein-induced lipid demixing in a membrane with interactions derived from experiment. Biophys J 101:1930–1937

    PubMed  CAS  Google Scholar 

  100. Johnson SA, Stinson BM, Go MS, Carmona LM, Reminick JI, Fang X, Baumgart T (2010) Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim Biophys Acta 1798:1427–1435

    PubMed  CAS  Google Scholar 

  101. Domon M, Matar G, Strzelecka-Kiliszek A, Bandorowicz-Pikula J, Pikula S, Besson F (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

    PubMed  CAS  Google Scholar 

  102. Li X, Becker KA, Zhang Y (2010) Ceramide in redox signaling and cardiovascular diseases. Cell Physiol Biochem. 26:41–48

    PubMed  Google Scholar 

  103. Schwarzer S, Nobles M, Tinker A (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

    PubMed  CAS  Google Scholar 

  104. Tobe T (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

    PubMed  CAS  Google Scholar 

  105. Ono A (2010) Relationships between plasma membrane microdomains and HIV-1 assembly. Biol Cell 102:335–350

    PubMed  CAS  Google Scholar 

  106. Vetrivel KS, Thinakaran G (2010) Membrane rafts in Alzheimer’s disease beta-amyloid production. Biochim Biophys Acta 1801:860–867

    PubMed  CAS  Google Scholar 

  107. Schengrund CL (2010) Lipid rafts: keys to neurodegeneration. Brain Res Bull 82:7–17

    PubMed  CAS  Google Scholar 

  108. Boini KM, Zhang C, Xia M, Han WQ, Brimson C, Poklis JL, Li PL (2010) Visfatin-induced lipid raft redox signaling platforms and dysfunction in glomerular endothelial cells. Biochim Biophys Acta 1801:1294–1304

    PubMed  CAS  Google Scholar 

  109. Murai T, Maruyama Y, Mio K, Nishiyama H, Suga M, Sato C (2011) Low cholesterol triggers membrane microdomain-dependent CD44 shedding and suppresses tumor cell migration. J Biol Chem 286:1999–2007

    PubMed  CAS  Google Scholar 

  110. Park EK, Lee EJ, Lee SH, Koo KH, Sung JY, Hwang EH, Park JH, Kim CW, Jeong KC, Park BK, Kim YN (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

    PubMed  CAS  Google Scholar 

  111. Staubach S, Hanisch FG (2011) Lipid rafts: signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics 8:263–277

    PubMed  CAS  Google Scholar 

  112. Assaife-Lopes N, Sousa VC, Pereira DB, Ribeiro JA, Chao MV, Sebastião AM (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

    PubMed  CAS  Google Scholar 

  113. Chichili GR, Westmuckett AD, Rodgers W (2010) T cell signal regulation by the actin cytoskeleton. J Biol Chem 285:14737–14746

    PubMed  CAS  Google Scholar 

  114. Ponce J, Brea D, Carrascal M, Guirao V, Degregorio-Rocasolano N, Sobrino T, Castillo J, Dávalos A, Gasull T (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

    PubMed  CAS  Google Scholar 

  115. Carrasco MP, Jiménez-López JM, Ríos-Marco P, Segovia JL, Marco C (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

    PubMed  CAS  Google Scholar 

  116. Pommier AJ, Alves G, Viennois E, Bernard S, Communal Y, Sion B, Marceau G, Damon C, Mouzat K, Caira F, Baron S, Lobaccaro JM (2010) Liver X Receptor activation downregulates AKT survival signaling in lipid rafts and induces apoptosis of prostate cancer cells. Oncogene 29:2712–2723

    PubMed  CAS  Google Scholar 

  117. Fuller M (2010) Sphingolipids: the nexus between Gaucher disease and insulin resistance. Lipids Health Dis 9:113

    PubMed  Google Scholar 

  118. Li X, Becker KA, Zhang Y (2010) Ceramide in redox signaling and cardiovascular diseases. Cell Physiol Biochem 26:41–48

    PubMed  Google Scholar 

  119. Stögbauer F, Weigert J, Neumeier M, Wanninger J, Sporrer D, Weber M, Schefler A, Enrich C, Wood P, Grewal T, Aslanidis C, Buechler C (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

    PubMed  Google Scholar 

  120. Sztolsztener ME, Strzelecka-Kiliszek A, Pikula S, Tylki-Szymanska A, Bandorowicz-Pikula J (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

    PubMed  Google Scholar 

  121. Domon MM, Besson F, Bandorowicz-Pikula J, Pikula S (2011) Annexin A6 is recruited into lipid rafts of Niemann-Pick type C disease fibroblasts in a Ca2+-dependent manner. Biochem Biophys Res Commun 405:192–196

    PubMed  CAS  Google Scholar 

  122. Schiffmann R (2010) Therapeutic approaches for neuronopathic lysosomal storage disorders. J Inherit Metab Dis 33:373–379

    PubMed  CAS  Google Scholar 

  123. Scott C, Ioannou YA (2004) The NPC1 protein: structure implies function. Biochim Biophys Acta 1685:8–13

    PubMed  CAS  Google Scholar 

  124. Blom TS, Linder MD, Snow K, Pihko H, Hess MW, Jokitalo E, Veckman V, Syvänen AC, Ikonen E (2003) Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann–Pick type C disease. Hum Mol Genet 12:257–272

    PubMed  CAS  Google Scholar 

  125. Ory DS (2000) Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim Biophys Acta 1529:331–339

    PubMed  CAS  Google Scholar 

  126. Ko DC, Binkley J, Sidow A, Scott MP (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

    PubMed  CAS  Google Scholar 

  127. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, Goldstein JL (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

    PubMed  CAS  Google Scholar 

  128. Mukherjee S, Maxfield F (2000) Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 1:203–211

    PubMed  CAS  Google Scholar 

  129. Vanier MT, Millat G (2003) Niemann–Pick disease type C. Clin Genet 64:269–281

    PubMed  CAS  Google Scholar 

  130. Chang TY, Reid PC, Sugii S, Ohgami N, Cruz JC, Chang CC (2005) Niemann–Pick type C disease and intracellular cholesterol trafficking. J Biol Chem 280:20917–20920

    PubMed  CAS  Google Scholar 

  131. Lange Y, Ye J, Rigney M, Steck TL (1999) Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40:2264–2270

    PubMed  CAS  Google Scholar 

  132. Troup GM, Wrenn SP (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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  134. te Vruchte D, Lloyd–Evans E, Veldman RJ, Neville DC, Dwek RA, Platt FM, van Blitterswijk WJ, Sillence DJ (2004) Accumulation of glycosphingolipids in Niemann–Pick C disease disrupts endosomal transport. J Biol Chem 279:26167–26175

    PubMed  CAS  Google Scholar 

  135. Cubells L, Vilà de Muga S, Tebar F, Wood P, Evans R, Ingelmo–Torres M, Calvo M, Gaus K, Pol A, Grewal T, Enrich C (2007) Annexin A6–induced alterations in cholesterol transport and caveolin export from the Golgi complex. Traffic 8:1568–1589

    PubMed  CAS  Google Scholar 

  136. Cubells L, Vilà de Muga S, Tebar F, Bonventre JV, Balsinde J, Pol A, Grewal T, Enrich C (2008) Annexin A6–induced inhibition of cytoplasmic phospholipase A2 is linked to caveolin–1 export from the Golgi. J Biol Chem 283:10174–10183

    PubMed  CAS  Google Scholar 

  137. Mayer G, Poirier S, Seidah NG (2008) Annexin A2 is a C-terminal PCSK9-binding protein that regulates endogenous low density lipoprotein receptor levels. J Biol Chem 283:31791–31801

    PubMed  CAS  Google Scholar 

  138. Davignon J, Dubuc G, Seidah NG (2010) The influence of PCSK9 polymorphisms on serum low-density lipoprotein cholesterol and risk of atherosclerosis. Curr Atheroscler Rep 12:308–315

    PubMed  CAS  Google Scholar 

  139. Valasek MA, Weng J, Shaul PW, Anderson RG, Repa JJ (2005) Caveolin-1 is not required for murine intestinal cholesterol transport. J Biol Chem 280:28103–28109

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

MD was a recipient of a stipend from the French Embassy in Warsaw. MNN and GM were recipients of PhD fellowships from the French Ministry of Higher Education and Research. The annexin-cholesterol project is supported in part by a grant NN401642740 from the National Science Center to JBP, by a grant NN401139839 from the Polish Ministry of Science and Higher Education to SP, by Polonium (JBP and FB), PICS (SP) and by CNRS (FB).

Author information

Authors and Affiliations

  1. Laboratory of Lipid Biochemistry, Department of Biochemistry, Nencki Institute of Experimental Biology, 3 Pasteur Street, 02-093, Warsaw, Poland

    Magdalena Domon & Slawomir Pikula

  2. Université de Lyon, 69622, Villeurbanne, France

    Magdalena Domon, Mehmet Nail Nasir, Gladys Matar & Françoise Besson

  3. Université Lyon 1, 69622, Villeurbanne, France

    Magdalena Domon, Mehmet Nail Nasir, Gladys Matar & Françoise Besson

  4. INSA de Lyon, 69622, Villeurbanne, France

    Magdalena Domon, Mehmet Nail Nasir, Gladys Matar & Françoise Besson

  5. CPE Lyon, 69616, Villeurbanne, France

    Magdalena Domon, Mehmet Nail Nasir, Gladys Matar & Françoise Besson

  6. ICBMS CNRS UMR 5246, 69622, Villeurbanne, France

    Magdalena Domon, Mehmet Nail Nasir, Gladys Matar & Françoise Besson

  7. Laboratory of Cellular Metabolism, Department of Biochemistry, Nencki Institute of Experimental Biology, 3 Pasteur Street, 02-093, Warsaw, Poland

    Joanna Bandorowicz-Pikula

Authors
  1. Magdalena Domon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mehmet Nail Nasir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gladys Matar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Slawomir Pikula
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Françoise Besson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joanna Bandorowicz-Pikula
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joanna Bandorowicz-Pikula.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Domon, M., Nasir, M.N., Matar, G. et al. Annexins as organizers of cholesterol- and sphingomyelin-enriched membrane microdomains in Niemann-Pick type C disease. Cell. Mol. Life Sci. 69, 1773–1785 (2012). https://doi.org/10.1007/s00018-011-0894-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-011-0894-0

Keywords

Search

Navigation