Fluid levity of the cell: Role of membrane lipid architecture in genetic sphingolipidoses

Journal of Neuroscience Research

Volumn 94, Issue 11, 2016, Pages 1019-1024

  D'Auria, Ludovic ^a   Bongarzone, Ernesto R ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

caveolin; fluidity; Krabbe's disease; lipid rafts; neurodegeneration; psychosine; sphingolipids

Indexed keywords

GLYCEROPHOSPHOLIPID; MEMBRANE LIPID; PHOSPHATICYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG;

BRAIN CELL; FLUORESCENCE MICROSCOPY; GLIA CELL; HEAD; HUMAN; LIPID RAFT; LIPID STORAGE; LIPIDOSIS; MEMBRANE FLUIDITY; MEMBRANE STABILIZATION; NEUROPATHOLOGY; NONHUMAN; NOTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SIGNAL TRANSDUCTION; SPHINGOLIPID METABOLISM;

EID: 84990191919     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23750     Document Type: Note

References (59)

1. Aureli M, Grassi S, Prioni S, Sonnino S, Prinetti A. 2015. Lipid membrane domains in the brain. Biochim Biophys Acta 1851:1006–1016.
2. Bagatolli LA. 2006. To see or not to see: lateral organization of biological membranes and fluorescence microscopy. Biochim Biophys Acta 1758:1541–1556.
3. Bagatolli LA, Ipsen JH, Simonsen AC, Mouritsen OG. 2010. An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog Lipid Res 49:378–389.
4. Bartke N, Hannun YA. 2009. Bioactive sphingolipids: metabolism and function. J Lipid Res 50(Suppl):S91–S96.
5. Baumgart T, Hammond AT, Sengupta P, Hess ST, Holowka DA, Baird BA, Webb WW. 2007. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci U S A 104:3165–3170.
6. Bernardino de la Serna J, Perez-Gil J, Simonsen AC, Bagatolli LA. 2004. Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J Biol Chem 279:40715–40722.
7. Byrne MC, Ledeen RW, Roisen FJ, Yorke G, Sclafani JR. 1983. Ganglioside-induced neuritogenesis: verification that gangliosides are the active agents and comparison of molecular species. J Neurochem 41:1214–1222.
8. Cantuti-Castelvetri L, Zhu H, Givogri MI, Chidavaenzi RL, Lopez-Rosas A, Bongarzone ER. 2012. Psychosine induces the dephosphorylation of neurofilaments by deregulation of PP1 and PP2A phosphatases. Neurobiol Dis 46:325–335.
9. Cantuti Castelvetri L, Givogri MI, Hebert A, Smith B, Song Y, Kaminska A, Lopez-Rosas A, Morfini G, Pigino G, Sands M, Brady ST, Bongarzone ER. 2013. The sphingolipid psychosine inhibits fast axonal transport in Krabbe disease by activation of GSK3β and deregulation of molecular motors. J Neurosci 33:10048–10056.
10. Carquin M, D‘Auria L, Pollet H, Bongarzone ER, Tyteca D. 2015. Recent progress on lipid lateral heterogeneity in plasma membranes: from rafts to submicrometric domains. Prog Lipid Res 62:1–24.
11. Castelvetri LC, Givogri MI, Zhu H, Smith B, Lopez-Rosas A, Qiu X, van Breemen R, Bongarzone ER. 2011. Axonopathy is a compounding factor in the pathogenesis of Krabbe disease. Acta Neuropathol 122:35–48.
12. Castro BM, Torreno-Pina JA, van Zanten TS, Gracia-Parajo MF. 2013. Biochemical and imaging methods to study receptor membrane organization and association with lipid rafts. Methods Cell Biol 117:105–122.
13. Castro BM, Prieto M, Silva LC. 2014. Ceramide: a simple sphingolipid with unique biophysical properties. Prog Lipid Res 54:53–67.
14. Cooke IR, Deserno M. 2006. Coupling between lipid shape and membrane curvature. Biophys J 91:487–495.
15. Cox TM, Cachon-Gonzalez MB. 2012. The cellular pathology of lysosomal diseases. J Pathol 226:241–254.
16. de Almeida RF, Fedorov A, Prieto M. 2003. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys J 85:2406–2416.
17. Devaux PF, Herrmann A, Ohlwein N, Kozlov MM. 2008. How lipid flippases can modulate membrane structure. Biochim Biophys Acta 1778:1591–1600.
18. Dietrich C, Bagatolli LA, Volovyk ZN, Thompson NL, Levi M, Jacobson K, Gratton E. 2001. Lipid rafts reconstituted in model membranes. Biophys J 80:1417–1428.
19. Fidorra M, Duelund L, Leidy C, Simonsen AC, Bagatolli LA. 2006. Absence of fluid-ordered/fluid-disordered phase coexistence in ceramide/POPC mixtures containing cholesterol. Biophys J 90:4437–4451.
20. Galvan C, Camoletto PG, Cristofani F, Van Veldhoven PP, Ledesma MD. 2008. Anomalous surface distribution of glycosyl phosphatidyl inositol-anchored proteins in neurons lacking acid sphingomyelinase. Mol Biol Cell 19:509–522.
21. Gomez-Mouton C, Lacalle RA, Mira E, Jimenez-Baranda S, Barber DF, Carrera AC, Martinez AC, Manes S. 2004. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J Cell Biol 164:759–768.
22. Goni FM, Alonso A, Bagatolli LA, Brown RE, Marsh D, Prieto M, Thewalt JL. 2008. Phase diagrams of lipid mixtures relevant to the study of membrane rafts. Biochim Biophys Acta 1781:665–684.
23. Gulbins E, Petrache I. 2013. Sphingolipids in disease. New York: Springer. p 478.
24. Hawkins-Salsbury JA, Parameswar AR, Jiang X, Schlesinger PH, Bongarzone E, Ory DS, Demchenko AV, Sands MS. 2013. Psychosine, the cytotoxic sphingolipid that accumulates in globoid cell leukodystrophy, alters membrane architecture. J Lipid Res 54:3303–3311.
25. Herring JM, McMichael MA, Smith SA. 2013. Microparticles in health and disease. J Vet Intern Med 27:1020–1033.
26. Iwabuchi K, Nakayama H, Iwahara C, Takamori K. 2010. Significance of glycosphingolipid fatty acid chain length on membrane microdomain-mediated signal transduction. FEBS Lett 584:1642–1652.
27. Jana A, Pahan K. 2010. Fibrillar amyloid-beta-activated human astroglia kill primary human neurons via neutral sphingomyelinase: implications for Alzheimer's disease. J Neurosci 30:12676–12689.
28. Kahya N, Scherfeld D, Bacia K, Poolman B, Schwille P. 2003. Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J Biol Chem 278:28109–28115.
29. Koberlin MS, Snijder B, Heinz LX, Baumann CL, Fauster A, Vladimer GI, Gavin AC, Superti-Furga G. 2015. A conserved circular network of coregulated lipids modulates innate immune responses. Cell 162:170–183.
30. Koike T, Ishida G, Taniguchi M, Higaki K, Ayaki Y, Saito M, Sakakihara Y, Iwamori M, Ohno K. 1998. Decreased membrane fluidity and unsaturated fatty acids in Niemann-Pick disease type C fibroblasts. Biochim Biophys Acta 1406:327–335.
31. Lenaz G. 1987. Lipid fluidity and membrane protein dynamics. Biosci Rep 7:823–837.
32. Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46–50.
33. McMahon HT, Boucrot E. 2015. Membrane curvature at a glance. J Cell Sci 128:1065–1070.
34. Mollinedo F, Gajate C. 2015. Lipid rafts as major platforms for signaling regulation in cancer. Adv Biol Regul 57:130–146.
35. Montes LR, Lopez DJ, Sot J, Bagatolli LA, Stonehouse MJ, Vasil ML, Wu BX, Hannun YA, Goni FM, Alonso A. 2008. Ceramide-enriched membrane domains in red blood cells and the mechanism of sphingomyelinase-induced hot-cold hemolysis. Biochemistry 47:11222–11230.
36. Munro S. 2003. Lipid rafts: elusive or illusive? Cell 115:377–388.
37. Nishio M, Fukumoto S, Furukawa K, Ichimura A, Miyazaki H, Kusunoki S, Urano T, Furukawa K. 2004. Overexpressed GM1 suppresses nerve growth factor (NGF) signals by modulating the intracellular localization of NGF receptors and membrane fluidity in PC12 cells. J Biol Chem 279:33368–33378.
38. Paintlia AS, Gilg AG, Khan M, Singh AK, Barbosa E, Singh I. 2003. Correlation of very-long-chain fatty acid accumulation and inflammatory disease progression in childhood X-ALD: implications for potential therapies. Neurobiol Dis 14:425–439.
39. Pinto SN, Silva LC, de Almeida RF, Prieto M. 2008. Membrane domain formation, interdigitation, and morphological alterations induced by the very-long-chain asymmetric C24:1 ceramide. Biophys J 95:2867–2879.
40. Pituch KC, Moyano AL, Lopez-Rosas A, Marottoli FM, Li G, Hu C, van Breemen R, Mansson JE, Givogri MI. 2015. Dysfunction of platelet-derived growth factor receptor alpha (PDGFRα) represses the production of oligodendrocytes from arylsulfatase A-deficient multipotential neural precursor cells. J Biol Chem 290:7040–7053.
41. Plasencia I, Norlen L, Bagatolli LA. 2007. Direct visualization of lipid domains in human skin stratum corneum ‘s lipid membranes: effect of pH and temperature. Biophys J 93:3142–3155.
42. Platt FM. 2014. Sphingolipid lysosomal storage disorders. Nature 510:68–75.
43. Prinetti A, Chigorno V, Prioni S, Loberto N, Marano N, Tettamanti G, Sonnino S. 2001. Changes in the lipid turnover, composition, and organization, as sphingolipid-enriched membrane domains, in rat cerebellar granule cells developing in vitro. J Biol Chem 276:21136–21145.
44. Purpura DP. 1978. Ectopic dendritic growth in mature pyramidal neurones in human ganglioside storage disease. Nature 276:520–521.
45. Purpura KP, Baker HJ. 1977. Neurite induction in mature cortical neurones in feline GM1-ganglioside storage disease. Nature 266:553–554.
46. Ramstedt B, Slotte JP. 2002. Membrane properties of sphingomyelins. FEBS Lett 531:33–37.
47. Saravanan K, Schaeren-Wiemers N, Klein D, Sandhoff R, Schwarz A, Yaghootfam A, Gieselmann V, Franken S. 2004. Specific downregulation and mistargeting of the lipid raft-associated protein MAL in a glycolipid storage disorder. Neurobiol Dis 16:396–406.
48. Scesa G, Moyano AL, Bongarzone ER, Givogri MI. 2016. Port-to-port delivery: mobilization of toxic sphingolipids via extracellular vesicles. J Neurosci Res 94:1333–1340.
49. Schulze H, Sandhoff K. 2011. Lysosomal lipid storage diseases. Cold Spring Harbor Perspect Biol 3.
50. Seyfried TN, Bernard DJ, Yu RK. 1984. Cellular distribution of gangliosides in the developing mouse cerebellum: analysis using the staggerer mutant. J Neurochem 43:1152–1162.
51. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569–572.
52. Singer SJ, Nicolson GL. 1972. The fluid mosaic model of the structure of cell membranes. Science 175:720–731.
53. Stancevic B, Kolesnick R. 2010. Ceramide-rich platforms in transmembrane signaling. FEBS Lett 584:1728–1740.
54. Suzuki K. 1998. Twenty-five years of the “psychosine hypothesis”: a personal perspective of its history and present status. Neurochem Res 23:251–259.
55. Trovo L, Stroobants S, D ‘Hooge R, Ledesma MD, Dotti CG. 2015. Improvement of biochemical and behavioral defects in the Niemann-Pick type A mouse by intraventricular infusion of MARCKS. Neurobiol Dis 73:319–326.
56. von Einem B, Weber P, Wagner M, Malnar M, Kosicek M, Hecimovic S, Arnim CA, Schneckenburger H. 2012. Cholesterol-dependent energy transfer between fluorescent proteins: insights into protein proximity of APP and BACE1 in different membranes in Niemann-Pick type C disease cells. Int J Mol Sci 13:15801–15812.
57. Westerlund B, Slotte JP. 2009. How the molecular features of glycosphingolipids affect domain formation in fluid membranes. Biochim Biophys Acta 1788:194–201.
58. White AB, Givogri MI, Lopez-Rosas A, Cao H, van Breemen R, Thinakaran G, Bongarzone ER. 2009. Psychosine accumulates in membrane microdomains in the brain of krabbe patients, disrupting the raft architecture. J Neurosci 29:6068–6077.
59. White AB, Galbiati F, Givogri MI, Lopez Rosas A, Qiu X, van Breemen R, Bongarzone ER. 2011. Persistence of psychosine in brain lipid rafts is a limiting factor in the therapeutic recovery of a mouse model for Krabbe disease. J Neurosci Res 89:352–364.