CoChat
Sign Up
Cited by 498

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles

Thiele, Christoph, Hannah, Matthew J., Fahrenholz, Falk, Huttner, Wieland B.·2000·Nature Cell Biology
DOI 10.1038/71366
Open this paper in CoChat — free account

Abstract

Here, to study lipid-protein interactions that contribute to the biogenesis of regulated secretory vesicles, we have developed new approaches by which to label proteins in vivo, using photoactivatable cholesterol and glycerophospholipids. We identify synaptophysin as a major specifically cholesterol-binding protein in PC12 cells and brain synaptic vesicles. Limited cholesterol depletion, which has little effect on total endocytic activity, blocks the biogenesis of synaptic-like microvesicles (SLMVs) from the plasma membrane. We propose that specific interactions between cholesterol and SLMV membrane proteins, such as synaptophysin, contribute to both the segregation of SLMV membrane constituents from plasma-membrane constituents, and the induction of synaptic-vesicle curvature.

Overview

Integrity signals

Registry

Crossref · 10.1038/71366

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The treatment decreased the number and size of muHTT aggregates and improved motor deficits in R6/2 mice and provided long-lasting improvement in zQ175 HD mice.

    “The treatment decreased the number and size of muHTT aggregates and improved motor deficits in R6/2 mice 54 and provided long-lasting improvement in zQ175 HD mice 56 .”

    From SREBP2 gene therapy targeting striatal astrocytes ameliorates Huntington’s disease phenotypes (2021) · cites this paper as [54]

  • The observed rescue in DRD2-MSNs, and in other synaptic features, may be favored by a closer contact between neurons and astrocytes, which is reduced in R6/2 astrocytes.

    “The observed rescue in DRD2-MSNs, and in other synaptic features, may be favored by a closer contact between neurons and astrocytes, which is reduced in R6/2 astrocytes 54 .”

    From SREBP2 gene therapy targeting striatal astrocytes ameliorates Huntington’s disease phenotypes (2021) · cites this paper as [54]

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 47

  1. Kirchhausen, T., Bonifacino, J. S. & Riezman, H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9, 488–495 (1997). · DOI
  2. Brown, D. & London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111–136 (1998). · DOI
  3. Thiele, C. & Huttner, W. B. Protein and lipid sorting from the trans-Golgi network to secretory granules — recent developments . Semin. Cell Dev. Biol. 9, 511– 516 (1998). · DOI
  4. Nickel, W., Bruegger, B. & Wieland, F. T. Protein and lipid sorting between the endoplasmatic reticulum and the Golgi complex. Semin. Cell Dev. Biol. 9, 493–502 (1998). · DOI
  5. Brown, D. A. & Rose, J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533– 544 (1992). · DOI · Paper page
  6. Radhakrishnan, R. et al. Phospholipids containing photoactivable groups in studies of biological membranes. Ann. NY Acad. Sci. 346, 165–198 (1980). · DOI
  7. Stoffel, W., Salm, K.-P. & Mueller, M. Syntheses of phosphatidylcholines, sphingomyelins and cholesterol substituted with azido fatty acids. Hoppe-Seylers Z. Physiol. Chem. 363, 1–18 (1982). · DOI
  8. Stoffel, W. & Metz, P. Covalent cross-linking of photosensitive phospholipids to human serum high density apolipoproteins (apoHDL). Hoppe-Seylers Z. Biol. Chem. 360, 197– 206 (1979). · DOI
  9. Westerman, J. et al. Identification of the lipid binding site of phosphatidylcholine-transfer protein with phosphatidylcholine analogs containing photoactivable carbene precursors. Eur. J. Biochem. 132, 441– 449 (1983). · DOI
  10. Pryde, J. G. & Phillips, J. H. Fractionation of membrane proteins by temperature-induced phase separation in Triton X-114. Biochem. J. 233, 525–533 ( 1986). · DOI
  11. Kurzchalia, T. V. et al. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J. Cell Biol. 118, 1003–1014 (1992). · DOI
  12. Murata, M. et al. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl Acad. Sci. USA 92, 10339– 10343 (1995). · DOI
  13. Ikonen, E. Molecular mechanisms of intracellular cholesterol transport. Curr. Opin. Lipidol. 8, 60–64 (1997). · DOI
  14. Iwata, S., Ostermeier, C., Ludwig, B. & Michel, H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660– 669 (1995). · DOI
  15. Tooze, S. A. & Huttner, W. B. Cell-free protein sorting to the regulated and constitutive secretory pathways. Cell 60, 837–847 (1990). · DOI
  16. Clift-O’Grady, L., Linstedt, A. D., Lowe, A. W., Grote, E. & Kelly, R. B. Biogenesis of synaptic vesicle-like structures in a pheochromocytoma cell line. J. Cell Biol. 110, 1693–1703 (1990). · DOI
  17. Corradi, N. et al. Overall lack of regulated secretion in a PC12 variant cell clone. J. Biol. Chem. 271, 27116– 27124 (1996). · DOI
  18. Finbow, M. E. & Harrison, M. A. The vacuolar H-ATPase: a universal proton pump. Biochem. J. 324, 697– 712 (1997). · DOI
  19. Jahn, R. & Südhof, T. C. Synaptic vesicles and exocytosis . Annu. Rev. Neurosci. 17, 219– 246 (1994). · DOI
  20. Bauerfeind, R., Jelinek, R. & Huttner, W. B. Synaptotagmin I- and II-deficient PC12 cells exhibit calcium-independent, depolarization-induced neurotransmitter release from synaptic-like microvesicles. FEBS Lett. 364, 328–334 (1995). · DOI
  21. Schmidt, A., Hannah, M. J. & Huttner, W. B. Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J. Cell Biol. 137 , 445–458 (1997). · DOI
  22. Lichtenstein, Y., Desnos, C., Fàundez, V., Kelly, R. B. & Clift-O’Grady, C. Vesiculation and sorting from PC12-derived endosomes in vitro. Proc. Natl Acad. Sci. USA 95, 11223–11228 ( 1998). · DOI
  23. Schmidt, A. & Huttner, W. B. Biogenesis of synaptic-like microvesicles in perforated PC12 cells. Methods: Companion to Methods Enzymol. 16, 160–169 ( 1998). · DOI
  24. Trowbridge, I. S., Collawn, J. F. & Hopkins, C. R. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9, 129–161 (1993). · DOI
  25. Evans, W. H. & Hardison, W. G. Phospholipid, cholesterol, polypeptide and glycoprotein composition of hepatic endosome subfractions. Biochem. J. 232, 33–36 ( 1985). · DOI
  26. Breckenridge, W. C., Morgan, I. G., Zanetta, J. P. & Vincendon, G. Adult rat brain synaptic vesicles. II. Lipid composition. Biochim. Biophys. Acta 320, 681–686 (1973). · DOI
  27. Perez-Castineira, J. R. & Apps, D. K. Vacuolar H(+)-ATPase of adrenal secretory granules. Rapid partial purification and reconstitution into proteoliposomes. Biochem. J. 271, 127 –131 (1990). · DOI
  28. Thomas, L. et al. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242, 1050–1053 (1988). · DOI
  29. Monier, S. et al. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell 6, 911–927 (1995). · DOI
  30. Rodal, S. K. et al. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961–974 ( 1999). · DOI
  31. Subtil, A. et al. Acute cholesterol depletion inhibits clathrin-coated pit budding . Proc. Natl Acad. Sci. USA 96, 6775– 6780 (1999). · DOI
  32. Keller, P. & Simons, K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140, 1357–1367 (1998). · DOI
  33. Ledesma, M. D., Simons, K. & Dotti, C. G. Neuronal polarity: essential role of protein-lipid complexes in axonal sorting. Proc. Natl Acad. Sci. USA 95, 3966–3971 (1998). · DOI
  34. Hannah, M. J., Weiss, U. & Huttner, W. B. Differential extraction of proteins from paraformaldehyde-fixed cells: lessons from synaptophysin and other membrane proteins. Methods: Companion to Methods Enzymol. 16, 170– 181 (1998). · DOI
  35. Brand, S. H. & Castle, J. D. SCAMP 37, a new marker within the general cell surface recycling system. EMBO J. 12, 3753–3761 (1993). · DOI
  36. Wu, T. T. & Castle, J. D. Evidence for colocalization and interaction between 37 and 39 kDa isoforms of secretory carrier membrane proteins (SCAMPs). J. Cell Sci. 110, 1533– 1541 (1997). · DOI
  37. Molday, R. S., Hicks, D. & Molday, L. Peripherin. A rim-specific membrane protein of rod outer segment discs. Invest. Ophthalmol. Vis. Sci. 28, 50–61 (1987).
  38. Goldberg, A. F. & Molday, R. S. Subunit composition of the peripherin/rds-rom-1 disk rim complex from rod photoreceptors: hydrodynamic evidence for a tetrameric quaternary structure. Biochemistry 35, 6144–6149 (1996). · DOI
  39. Church, R. F. R. & Weiss, M. J. Diazirines. II. Synthesis and properties of small functionalized diazirine molecules. Some observations on the reaction of a diaziridine with the iodine-iodide ion system . J. Org. Chem. 35, 2465– 2471 (1970). · DOI
  40. Spector, A. A. & Hoak, J. C. An improved method for the addition of long-chain free fatty acid to protein solutions. Anal. Biochem. 32, 297–302 (1969). · DOI
  41. Beisswanger, R. et al. Existence of distinct tyrosylprotein sulfotransferase genes: molecular characterization of tyrosylprotein sulfotransferase-2. Proc. Natl Acad. Sci. USA 95, 11134– 11139 (1998). · DOI
  42. Huttner, W. B., Schiebler, W., Greengard, P. & De Camilli, P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374– 1388 (1983). · DOI
  43. Baumert, M., Maycox, P.R., Navone, F., De Camilli, P. & Jahn, R. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 8, 379–384 ( 1989). · DOI
  44. Heumann, R., Kachel, V. & Thoenen, H. Relationship between NGF-mediated volume increase and “priming effect” in fast and slow reacting clones of PC12 pheochromocytoma cells. Exp. Cell Res. 145, 179– 190 (1983). · DOI
  45. Pimplikar, S., Ikonen, E. & Simons, K. Basolateral protein transport in streptolysin O-permeabilized MDCK cells. J. Cell Biol. 125, 1025– 1035 (1994). · DOI
  46. Zacchetti, D., Peränen, J., Murata, M., Fiedler, K. & Simons, K. VIP17-MAL, a proteolipid in apical transport vesicles. FEBS Lett. 377, 465– 469 (1995). · DOI
  47. Klein, U., Gimpl, G. & Fahrenholz, F. Alteration of the myometrial plasma membrane cholesterol content with beta cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 34, 13784– 13793 (1995). · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Thiele, C., Hannah, M. J., Fahrenholz, F., & Huttner, W. B.
Venue
Nature Cell Biology
Publisher
Springer Science and Business Media LLC
Published
1999-12-10
Volume
2
Issue
1
Pages
42-49
ISSN
  • 1465-7392
  • 1476-4679
DOI
10.1038/71366
Cited by
498
References
1
Language
en
Licence
www.springer.com/tdm (tdm)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review