Structural insights into the organization of the cavin membrane coat complex

Developmental Cell

Volumn 31, Issue 4, 2014, Pages 405-419

  Kovtun, Oleksiy ^a   Tillu, Vikas A ^a   Jung, WooRam ^a   Leneva, Natalya ^a   Ariotti, Nicholas ^a   Chaudhary, Natasha ^a   Mandyam, Ramya A ^a   Ferguson, Charles ^a   Morgan, Garry P ^a   Johnston, Wayne A ^a   Harrop, Stephen J ^b,c   Alexandrov, Kirill ^a   Parton, Robert G ^a   Collins, Brett M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c AUSTRALIAN SYNCHROTRON   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAVIN1; CAVIN4A; MEMBRANE PROTEIN; POLYPHOSPHOINOSITIDE; UNCLASSIFIED DRUG; CAVEOLIN; RNA BINDING PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CAVEOLA; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; HELICAL REGION 1 DOMAIN; MEMBRANE BINDING; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SURFACE PROPERTY; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOPLASM; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; CAVEOLAE; CAVEOLINS; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, QUATERNARY; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84921310508     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.002     Document Type: Article

References (43)

1. Bastiani M., Liu L., Hill M.M., Jedrychowski M.P., Nixon S.J., Lo H.P., Abankwa D., Luetterforst R., Fernandez-Rojo M., Breen M.R., et al. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J.Cell Biol. 2009, 185:1259-1273.
2. Breen M.R., Camps M., Carvalho-Simoes F., Zorzano A., Pilch P.F. Cholesterol depletion in adipocytes causes caveolae collapse concomitant with proteosomal degradation of cavin-2 in a switch-like fashion. PLoS ONE 2012, 7:e34516.
3. Burgener R., Wolf M., Ganz T., Baggiolini M. Purification and characterization of a major phosphatidylserine-binding phosphoprotein from human platelets. Biochem. J. 1990, 269:729-734.
4. Ciani B., Bjelic S., Honnappa S., Jawhari H., Jaussi R., Payapilly A., Jowitt T., Steinmetz M.O., Kammerer R.A. Molecular basis of coiled-coil oligomerization-state specificity. Proc. Natl. Acad. Sci. USA 2010, 107:19850-19855.
5. Conners R., Hill D.J., Borodina E., Agnew C., Daniell S.J., Burton N.M., Sessions R.B., Clarke A.R., Catto L.E., Lammie D., et al. The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled-coil. EMBO J. 2008, 27:1779-1789.
6. Fernandez I., Ying Y., Albanesi J., Anderson R.G. Mechanism of caveolin filament assembly. Proc. Natl. Acad. Sci. USA 2002, 99:11193-11198.
7. Folta-Stogniew E., Williams K.R. Determination of molecular masses of proteins in solution: Implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory. J.Biomol. Tech. 1999, 10:51-63.
8. Fra A.M., Williamson E., Simons K., Parton R.G. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA 1995, 92:8655-8659.
9. Fujita A., Cheng J., Tauchi-Sato K., Takenawa T., Fujimoto T. A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc. Natl. Acad. Sci. USA 2009, 106:9256-9261.
10. Gambin Y., Ariotti N., McMahon K.A., Bastiani M., Sierecki E., Kovtun O., Polinkovsky M.E., Magenau A., Jung W., Okano S., et al. Single-molecule analysis reveals self assembly and nanoscale segregation of two distinct cavin subcomplexes on caveolae. eLife 2014, 3:e01434.
11. Gustincich S., Schneider C. Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell growth & differentiation: the molecular biology journal of the American Association for Cancer Research 1993, 4:753-760.
12. Gustincich S., Vatta P., Goruppi S., Wolf M., Saccone S., Della Valle G., Baggiolini M., Schneider C. The human serum deprivation response gene (SDPR) maps to 2q32-q33 and codes for a phosphatidylserine-binding protein. Genomics 1999, 57:120-129.
13. Hailstones D., Sleer L.S., Parton R.G., Stanley K.K. Regulation of caveolin and caveolae by cholesterol in MDCK cells. J.Lipid Res. 1998, 39:369-379.
14. Hansen C.G., Nichols B.J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol. 2010, 20:177-186.
15. Hansen C.G., Bright N.A., Howard G., Nichols B.J. SDPR induces membrane curvature and functions in the formation of caveolae. Nat. Cell Biol. 2009, 11:807-814.
16. Hansen C.G., Shvets E., Howard G., Riento K., Nichols B.J. Deletion of cavin genes reveals tissue-specific mechanisms for morphogenesis of endothelial caveolae. Nat. Commun. 2013, 4:1831.
17. Hartmann M.D., Ridderbusch O., Zeth K., Albrecht R., Testa O., Woolfson D.N., Sauer G., Dunin-Horkawicz S., Lupas A.N., Alvarez B.H. A coiled-coil motif that sequesters ions to the hydrophobic core. Proc. Natl. Acad. Sci. USA 2009, 106:16950-16955.
18. Hartmann M.D., Grin I., Dunin-Horkawicz S., Deiss S., Linke D., Lupas A.N., Hernandez Alvarez B. Complete fiber structures of complex trimeric autotransporter adhesins conserved in enterobacteria. Proc. Natl. Acad. Sci. USA 2012, 109:20907-20912.
19. Hayer A., Stoeber M., Bissig C., Helenius A. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 2010, 11:361-382.
20. Hill M.M., Bastiani M., Luetterforst R., Kirkham M., Kirkham A., Nixon S.J., Walser P., Abankwa D., Oorschot V.M., Martin S., et al. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 2008, 132:113-124.
21. Holm L., Rosenström P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010, 38. W545-9.
22. Humphrey S.J., Yang G., Yang P., Fazakerley D.J., Stöckli J., Yang J.Y., James D.E. Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2. Cell Metab. 2013, 17:1009-1020.
23. Izumi Y., Hirai Si., Tamai Y., Fujise-Matsuoka A., Nishimura Y., Ohno S. A protein kinase Cdelta-binding protein SRBC whose expression is induced by serum starvation. J.Biol. Chem. 1997, 272:7381-7389.
24. Kovtun O., Mureev S., Jung W., Kubala M.H., Johnston W., Alexandrov K. Leishmania cell-free protein expression system. Methods 2011, 55:58-64.
25. Lanzafame A.A., Turnbull L., Amiramahdi F., Arthur J.F., Huynh H., Woodcock E.A. Inositol phospholipids localized to caveolae in rat heart are regulated by alpha1-adrenergic receptors and by ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H2059-H2065.
26. Liu L., Brown D., McKee M., Lebrasseur N.K., Yang D., Albrecht K.H., Ravid K., Pilch P.F. Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab. 2008, 8:310-317.
27. Ludwig A., Howard G., Mendoza-Topaz C., Deerinck T., Mackey M., Sandin S., Ellisman M.H., Nichols B.J. Molecular composition and ultrastructure of the caveolar coat complex. PLoS Biol. 2013, 11:e1001640.
28. Matsuoka K., Schekman R. The use of liposomes to study COPII- and COPI-coated vesicle formation and membrane protein sorting. Methods 2000, 20:417-428.
29. McMahon K.A., Zajicek H., Li W.P., Peyton M.J., Minna J.D., Hernandez V.J., Luby-Phelps K., Anderson R.G. SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J. 2009, 28:1001-1015.
30. Mineo C., Ying Y.S., Chapline C., Jaken S., Anderson R.G. Targeting of protein kinase Calpha to caveolae. J.Cell Biol. 1998, 141:601-610.
31. Mureev S., Kovtun O., Nguyen U.T., Alexandrov K. Species-independent translational leaders facilitate cell-free expression. Nat. Biotechnol. 2009, 27:747-752.
32. Murray D.H., Tamm L.K. Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 2009, 48:4617-4625.
33. Palade G.E. Fine structure of blood capillaries. J.Appl. Physiol. 1953, 24:1424.
34. Parton R.G., del Pozo M.A. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 2013, 14:98-112.
35. Peters K.R., Carley W.W., Palade G.E. Endothelial plasmalemmal vesicles have a characteristic striped bipolar surface structure. J.Cell Biol. 1985, 101:2233-2238.
36. Rothberg K.G., Heuser J.E., Donzell W.C., Ying Y.S., Glenney J.R., Anderson R.G. Caveolin, a protein component of caveolae membrane coats. Cell 1992, 68:673-682.
37. Sinha B., Köster D., Ruez R., Gonnord P., Bastiani M., Abankwa D., Stan R.V., Butler-Browne G., Vedie B., Johannes L., et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011, 144:402-413.
38. Steinmetz M.O., Jelesarov I., Matousek W.M., Honnappa S., Jahnke W., Missimer J.H., Frank S., Alexandrescu A.T., Kammerer R.A. Molecular basis of coiled-coil formation. Proc. Natl. Acad. Sci. USA 2007, 104:7062-7067.
39. Walser P.J., Ariotti N., Howes M., Ferguson C., Webb R., Schwudke D., Leneva N., Cho K.J., Cooper L., Rae J., et al. Constitutive formation of caveolae in a bacterium. Cell 2012, 150:752-763.
40. Westermann M., Steiniger F., Richter W. Belt-like localisation of caveolin in deep caveolae and its re-distribution after cholesterol depletion. Histochem. Cell Biol. 2005, 123:613-620.
41. Yamada E. The fine structure of the gall bladder epithelium of the mouse. J.Biophys. Biochem. Cytol. 1955, 1:445-458.
42. Yang P., Patrick E., Tan S.X., Fazakerley D.J., Burchfield J., Gribben C., Prior M.J., James D.E., Hwa Yang Y. Direction pathway analysis of large-scale proteomics data reveals novel features of the insulin action pathway. Bioinformatics 2014, 30:808-814.
43. Zhang J., Xiao P., Zhang X. Phosphatidylserine externalization in caveolae inhibits Ca2+ efflux through plasma membrane Ca2+-ATPase in ECV304. Cell Calcium 2009, 45:177-184.