Biogenesis of caveolae: Stepwise assembly of large caveolin and cavin complexes

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Volumn 11, Issue 3, 2010, Pages 361-382

  Hayer, Arnold ^a   Stoeber, Miriam ^a   Bissig, Christin ^a,b   Helenius, Ari ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Caveolae; Caveolin; Cavin; ER; Exocytosis; GFP GPI; Golgi; PTRF; Secretory pathway; VSVG

Indexed keywords

CAVEOLIN 1; CAVEOLIN 2; CAVIN 1; DYNAMIN II; MEMBRANE PROTEIN; POLYMERASE I AND TRANSCRIPT RELEASE FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CAVEOLA; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE SILENCING; GENETIC ASSOCIATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; CAVEOLAE; CAVEOLIN 1; CAVEOLIN 2; CELLS, CULTURED; CHOLESTEROL; ENDOPLASMIC RETICULUM; GLYCOSYLPHOSPHATIDYLINOSITOLS; GOLGI APPARATUS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; RNA-BINDING PROTEINS;

EID: 77949557277     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.01023.x     Document Type: Article

References (60)

1. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007, 8:185-194.
2. Tagawa A, Mezzacasa A, Hayer A, Longatti A, Pelkmans L, Helenius A. Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J Cell Biol 2005, 170:769-779.
3. Fra AM, Williamson E, Simons K, Parton RG. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 1995, 92:8655-8659.
4. Capozza F, Cohen AW, Cheung MW, Sotgia F, Schubert W, Battista M, Lee H, Frank PG, Lisanti MP. Muscle-specific interaction of caveolin isoforms: differential complex formation between caveolins in fibroblastic vs. muscle cells. Am J Physiol Cell Physiol 2005, 288:C677-C691.
5. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A 1995, 92:10339-10343.
6. Scherer PE, Okamoto T, Chun M, Nishimoto I, Lodish HF, Lisanti MP. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc Natl Acad Sci U S A 1996, 93:131-135.
7. Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J Cell Biol 1998, 140:795-806.
8. Kirkham M, Nixon SJ, Howes MT, Abi-Rached L, Wakeham DE, Hanzal-Bayer M, Ferguson C, Hill MM, Fernandez-Rojo M, Brown DA, Hancock JF, Brodsky FM, Parton RG. Evolutionary analysis and molecular dissection of caveola biogenesis. J Cell Sci 2008, 121:2075-2086.
9. Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, Lo HP, Abankwa D, Luetterforst R, Fernandez-Rojo M, Breen MR, Gygi SP, Vinten J, Walser PJ, North KN, Hancock JF. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 2009, 185:1259-1273.
10. Hansen CG, Bright NA, Howard G, Nichols BJ. SDPR induces membrane curvature and functions in the formation of caveolae. Nat Cell Biol 2009, 11:807-814.
11. McMahon KA, Zajicek H, Li WP, Peyton MJ, Minna JD, Hernandez VJ, Luby-Phelps K, Anderson RG. SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. Embo J 2009, 28:1001-1015.
12. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, Hancock JF, Parton RG. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 2008, 132:113-124.
13. Liu L, Pilch PF. A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 2008, 283:4314-4322.
14. Monier S, Parton RG, Vogel F, Behlke J, Henske A, Kurzchalia TV. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 1995, 6:911-927.
15. Fernandez I, Ying Y, Albanesi J, Anderson RG. Mechanism of caveolin filament assembly. Proc Natl Acad Sci U S A 2002, 99:11193-11198. Epub 12002 Aug 11197.
16. Sargiacomo M, Scherer PE, Tang Z, Kubler E, Song KS, Sanders MC, Lisanti MP. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci U S A 1995, 92:9407-9411.
17. Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, Lisanti MP. Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 1997, 272:29337-29346.
18. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, Rodriguez-Boulan E. Caveolin-2 localizes to the golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 1999, 274:25708-25717.
19. Parolini I, Sargiacomo M, Galbiati F, Rizzo G, Grignani F, Engelman JA, Okamoto T, Ikezu T, Scherer PE, Mora R, Rodriguez-Boulan E, Peschle C, Lisanti MP. Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the golgi complex. J Biol Chem 1999, 274:25718-25725.
20. Aboulaich N, Vainonen JP, Stralfors P, Vener AV. Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem J 2004, 383:237-248.
21. Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J. Identification of a major protein on the cytosolic face of caveolae. Biochim Biophys Acta 2005, 1717:34-40.
22. Liu L, Brown D, McKee M, Lebrasseur NK, Yang D, Albrecht KH, Ravid K, Pilch PF. Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab 2008, 8:310-317.
23. Nishimura N, Balch WE. A di-acidic signal required for selective export from the endoplasmic reticulum. Science 1997, 277:556-558.
24. Nishimura N, Bannykh S, Slabough S, Matteson J, Altschuler Y, Hahn K, Balch WE. A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J Biol Chem 1999, 274:15937-15946.
25. Sevier CS, Weisz OA, Davis M, Machamer CE. Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol Biol Cell 2000, 11:13-22.
26. Votsmeier C, Gallwitz D. An acidic sequence of a putative yeast Golgi membrane protein binds COPII and facilitates ER export. Embo J 2001, 20:6742-6750.
27. Brown WJ, Plutner H, Drecktrah D, Judson BL, Balch WE. The lysophospholipid acyltransferase antagonist CI-976 inhibits a late step in COPII vesicle budding. Traffic 2008, 9:786-797.
28. Lee H, Park DS, Razani B, Russell RG, Pestell RG, Lisanti MP. Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am J Pathol 2002, 161:1357-1369.
29. Machleidt T, Li WP, Liu P, Anderson RG. Multiple domains in caveolin-1 control its intracellular traffic. J Cell Biol 2000, 148(1):17-28.
30. Pol A, Martin S, Fernandez MA, Ingelmo-Torres M, Ferguson C, Enrich C, Parton RG. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol Biol Cell 2005, 16:2091-2105.
31. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992, 68:673-682.
32. Cubells L, Vila de Muga S, Tebar F, Wood P, Evans R, Ingelmo-Torres M, Calvo M, Gaus K, Pol A, Grewal T, Enrich C. Annexin A6-induced alterations in cholesterol transport and caveolin export from the Golgi complex. Traffic 2007, 8:1568-1589.
33. Pelkmans L, Zerial M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 2005, 436:128-133.
34. Keller P, Toomre D, Diaz E, White J, Simons K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat Cell Biol 2001, 3:140-149.
35. Kreitzer G, Marmorstein A, Okamoto P, Vallee R, Rodriguez-Boulan E. Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat Cell Biol 2000, 2:125-127.
36. Liu YW, Surka MC, Schroeter T, Lukiyanchuk V, Schmid SL. Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol Biol Cell 2008, 19:5347-5359.
37. Bonazzi M, Spano S, Turacchio G, Cericola C, Valente C, Colanzi A, Kweon HS, Hsu VW, Polishchuck EV, Polishchuck RS, Sallese M, Pulvirenti T, Corda D, Luini A. CtBP3/BARS drives membrane fission in dynamin-independent transport pathways. Nat Cell Biol 2005, 7:570-580.
38. Cao H, Weller S, Orth JD, Chen J, Huang B, Chen JL, Stamnes M, McNiven MA. Actin and Arf1-dependent recruitment of a cortactin-dynamin complex to the Golgi regulates post-Golgi transport. Nat Cell Biol 2005, 7:483-492. Epub 2005 Apr 2010.
39. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 2006, 10:839-850.
40. Godi A, Di Campli A, Konstantakopoulos A, Di Tullio G, Alessi DR, Kular GS, Daniele T, Marra P, Lucocq JM, De Matteis MA. FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat Cell Biol 2004, 6:393-404.
41. Vieira OV, Verkade P, Manninen A, Simons K. FAPP2 is involved in the transport of apical cargo in polarized MDCK cells. J Cell Biol 2005, 170:521-526.
42. Wanaski SP, Ng BK, Glaser M. Caveolin scaffolding region and the membrane binding region of SRC form lateral membrane domains. Biochemistry 2003, 42:42-56.
43. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, Lisanti MP. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 1996, 271:2255-2261.
44. Ren X, Ostermeyer AG, Ramcharan LT, Zeng Y, Lublin DM, Brown DA. Conformational defects slow Golgi exit, block oligomerization, and reduce raft affinity of caveolin-1 mutant proteins. Mol Biol Cell 2004, 15:4556-4567.
45. Ostermeyer AG, Paci JM, Zeng Y, Lublin DM, Munro S, Brown DA. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J Cell Biol 2001, 152:1071-1078.
46. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, Parton RG. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 2001, 152:1057-1070.
47. Choudhury A, Marks DL, Proctor KM, Gould GW, Pagano RE. Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface. Nat Cell Biol 2006, 8:317-328.
48. 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.
49. Nabi IR. Cavin fever: regulating caveolae. Nat Cell Biol 2009, 11:789-791.
50. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452. Epub 2001 Aug 2449.
51. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002, 296:913-916.
52. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001, 3:473-483.
53. Solis GP, Hoegg M, Munderloh C, Schrock Y, Malaga-Trillo E, Rivera-Milla E, Stuermer CA. Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. Biochem J 2007, 403:313-322.
54. Cao H, Garcia F, McNiven MA. Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 1998, 9:2595-2609.
55. Lee E, De Camilli P. Dynamin at actin tails. Proc Natl Acad Sci U S A 2002, 99:161-166.
56. Balla A, Tuymetova G, Tsiomenko A, Varnai P, Balla T. A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol Biol Cell 2005, 16:1282-1295.
57. Sohda M, Misumi Y, Yoshimura S, Nakamura N, Fusano T, Sakisaka S, Ogata S, Fujimoto J, Kiyokawa N, Ikehara Y. Depletion of vesicle-tethering factor p115 causes mini-stacked Golgi fragments with delayed protein transport. Biochem Biophys Res Commun 2005, 338:1268-1274.
58. Thevenaz P, Ruttimann UE, Unser M. A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 1998, 7:27-41.
59. Phair RD, Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 2000, 404:604-609.
60. Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K, Helenius A. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 2007, 131:516-529.