Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 8, 2013, Pages

  Frisz, Jessica F ^a   Lou, Kaiyan ^a   Klitzing, Haley A ^a   Hanafin, William P ^a   Lizunov, Vladimir ^b   Wilson, Robert L ^a   Carpenter, Kevin J ^c   Kim, Raehyun ^a   Hutcheon, Ian D ^c   Zimmerberg, Joshua ^b   Weber, Peter K ^c   Kraft, Mary L ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

SIMS; Stable isotope

Indexed keywords

CARBON 13; CERAMIDE; CHOLESTEROL; GLYCOSPHINGOLIPID; HEMAGGLUTININ; ION; NITROGEN 15; SPHINGOLIPID; SPHINGOMYELIN;

ANIMAL CELL; ARTICLE; ARTIFACT; CELL LABELING; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYTOSKELETON; FIBROBLAST; LIPID RAFT; LIPOLYSIS; MASS SPECTROMETRY; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY;

CELL MEMBRANE; FIBROBLASTS; HEMAGGLUTININS; MEMBRANE LIPIDS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; SPECTROMETRY, MASS, SECONDARY ION; SPHINGOLIPIDS;

EID: 84874242588     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1216585110     Document Type: Article

References (52)

1. Radhakrishnan K, Halász A, Vlachos D, Edwards JS (2010) Quantitative understanding of cell signaling: The importance of membrane organization. Curr Opin Biotechnol 21 (5):677-682.
2. Karnovsky MJ, Kleinfeld AM, Hoover RL, Klausner RD (1982) The concept of lipid domains in membranes. J Cell Biol 94 (1):1-6.
3. Douglass AD, Vale RD (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 121 (6):937-950.
4. Fujita A, Cheng J, Fujimoto T (2009) Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim Biophys Acta 1791 (5):388-396.
5. Neumann AK, Itano MS, Jacobson K (2010) Understanding lipid rafts and other related membrane domains. F1000 Biol Rep 2:31.
6. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: New tools and insights. Nat Rev Mol Cell Biol 11 (10):688-699.
7. Jacobson K, Mouritsen OG, Anderson RGW (2007) Lipid rafts: At a crossroad between cell biology and physics. Nat Cell Biol 9 (1):7-14.
8. Shaw AS (2006) Lipid rafts: Now you see them, now you don't. Nat Immunol 7 (11):1139-1142.
9. Leslie M (2011) Mysteries of the cell. Do lipid rafts exist? Science 334 (6059):1046-1047.
10. Hess ST, et al. (2005) Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin. J Cell Biol 169 (6):965-976.
11. Polozov IV, Bezrukov L, Gawrisch K, Zimmerberg J (2008) Progressive ordering with decreasing temperature of the phospholipids of influenza virus. Nat Chem Biol 4 (4):248-255.
12. Scheiffele P, Roth MG, Simons K (1997) Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J 16 (18):5501-5508.
13. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: Lessons from sphingolipids. Nat Rev Mol Cell Biol 9 (2):139-150.
14. McMahon G, Glassner BJ, Lechene CP (2006) Quantitative imaging of cells with multi-isotope imaging mass spectrometry (MIMS)-Nanoautography with stable isotope tracers. Appl Surf Sci 252 (19):6895-6906.
15. Boxer SG, Kraft ML, Weber PK (2009) Advances in imaging secondary ion mass spectrometry for biological samples. Annu Rev Biophys 38 (1):53-74.
16. Lechene C, et al. (2006) High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J Biol 5 (6):20.
17. Anderton CR, Lou K, Weber PK, Hutcheon ID, Kraft ML (2011) Correlated AFM and NanoSIMS imaging to probe cholesterol-induced changes in phase behavior and non-ideal mixing in ternary lipid membranes. Biochim Biophys Acta 1808 (1):307-315.
18. Kraft ML, Weber PK, Longo ML, Hutcheon ID, Boxer SG (2006) Phase separation of lipid membranes analyzed with high-resolution secondary ion mass spectrometry. Science 313 (5795):1948-1951.
19. Steinhauser ML, et al. (2012) Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature 481 (7382):516-519.
20. Chigorno V, et al. (1997) Metabolic processing of gangliosides by human fibroblasts in culture-formation and recycling of separate pools of sphingosine. Eur J Biochem 250 (3):661-669.
21. Wilson RL, et al. (2012) Fluorinated colloidal gold immunolabels for imaging select proteins in parallel with lipids using high-resolution secondary ion mass spectrometry. Bioconjug Chem 23 (3):450-460.
22. Cheng J, et al. (2009) Quantitative electron microscopy shows uniform incorporation of triglycerides into existing lipid droplets. Histochem Cell Biol 132 (3):281-291.
23. Altelaar AFM, et al. (2006) Gold-enhanced biomolecular surface imaging of cells and tissue by SIMS and MALDI mass spectrometry. Anal Chem 78 (3):734-742.
24. Lechene CP, Luyten Y, McMahon G, Distel DL (2007) Quantitative imaging of nitrogen fixation within animal cells. Science 317:1563-1566.
25. Klitzing HA, Weber PK, Kraft ML (2013) Secondary ion mass spectrometry imaging of biological membranes at high spatial resolution. Nanoimaging: Methods and Protocols, Methods in Molecular Biology, eds Sousa AA, Kruhlak MJ (Humana Press, Totowa, NJ), Vol 950, pp483-501.
26. Ghosal S, et al. (2008) Imaging and 3D elemental characterization of intact bacterial spores by high-resolution secondary ion mass spectrometry. Anal Chem 80 (15):5986-5992.
27. Edidin M (2003) Lipids on the frontier: A century of cell-membrane bilayers. Nat Rev Mol Cell Biol 4 (5):414-418.
28. 1 integrin-mediated adhesive contacts in motile fibroblasts. J Cell Biol 119 (5):1347-1359.
29. Chen Y, Qin J, Cai J, Chen ZW (2009) Cold induces micro-and nano-scale reorganization of lipid raft markers at mounds of T-cell membrane fluctuations. PLoS ONE 4 (4):e5386.
30. Feigenson GW (2007) Phase boundaries and biological membranes. Annu Rev Biophys Biomol Struct 36 (1):63-77.
31. Sun M, et al. (2007) The effect of cellular cholesterol on membrane-cytoskeleton adhesion. J Cell Sci 120 (Pt 13):2223-2231.
32. Kwik J, et al. (2003) Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4, 5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100 (24):13964-13969.
33. Qi M, Liu Y, Freeman MR, Solomon KR (2009) Cholesterol-regulated stress fiber formation. J Cell Biochem 106 (6):1031-1040.
34. Spector I, Shochet NR, Kashman Y, Groweiss A (1983) Latrunculins: Novel marine toxins that disrupt microfilament organization in cultured cells. Science 219 (4584):493-495.
35. Kenworthy AK, et al. (2004) Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165 (5):735-746.
36. Fujita A, et al. (2007) Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol Biol Cell 18 (6):2112-2122.
37. Chen Y, Qin J, Chen ZW (2008) Fluorescence-topographic NSOM directly visualizes peak-valley polarities of GM1/GM3 rafts in cell membrane fluctuations. J Lipid Res 49 (10):2268-2275.
38. Pralle A, Keller P, Florin EL, Simons K, Hörber JK (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148 (5):997-1008.
39. Lasserre R, et al. (2008) Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 4 (9):538-547.
40. Eggeling C, et al. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457 (7233):1159-1162.
41. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157 (6):1071-1081.
42. Goswami D, et al. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135 (6):1085-1097.
43. Mueller V, et al. (2011) STED nanoscopy reveals molecular details of cholesterol-and cytoskeleton-modulated lipid interactions in living cells. Biophys J 101 (7):1651-1660.
44. Gowrishankar K, et al. (2012) Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149 (6):1353-1367.
45. Tyteca D, et al. (2010) Three unrelated sphingomyelin analogs spontaneously cluster into plasma membrane micrometric domains. Biochim Biophys Acta 1798 (5):909-927.
46. Fujimoto T (1996) GPI-anchored proteins, glycosphingolipids, and sphingomyelin are sequestered to caveolae only after crosslinking. J Histochem Cytochem 44 (8):929-941.
47. Marks DL, Bittman R, Pagano RE (2008) Use of Bodipy-labeled sphingolipid and cholesterol analogs to examine membrane microdomains in cells. Histochem Cell Biol 130 (5):819-832.
48. Kusumi A, et al. (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34 (1):351-378.
49. Carner P, Park JM, Malecki E (1998) A stereodivergent synthesis of D-erythro-sphingosine and D-threo-sphingosine from L-serine. J Org Chem 53 (18):4395-4398.
50. Dondoni A, Perrone D (2000) Synthesis of 1, 1-dimethylethyl (S)-4-formyl-2, 2-dimethyl-3-oxazolidinecarboxylate by oxidation of the alcohol. Org Synth 77:64-77.
51. Peters C, et al. (2007) Synthesis of borondipyrromethene (BODIPY)-labeled sphingosine derivatives by cross-metathesis reaction. J Org Chem 72 (5):1842-1845.
52. Stenkula KG, Lizunov VA, Cushman SW, Zimmerberg J (2010) Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab 12 (3):250-259.