Clathrin-independent pathways of endocytosis

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 6, 2014, Pages

  Mayor, Satyajit ^a   Parton, Robert G ^b   Donaldson, Julie G ^c  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; DYNAMIN;

CELL MEMBRANE; ENDOCYTOSIS; METABOLISM; PHYSIOLOGY;

CELL MEMBRANE; CLATHRIN; DYNAMINS; ENDOCYTOSIS;

EID: 84889073868     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016758     Document Type: Article

References (157)

1. Allaire PD, Seyed Sadr M, Chaineau M, Seyed Sadr E, Konefal S, Fotouhi M, Maret D, Ritter B, Del Maestro RF, McPherson PS. 2013. Interplay between Rab35 and Arf6 controls cargo recycling to coordinate cell adhesion and migration. J Cell Sci 126: 722-731.
2. Anderson HA, Chen Y, Norkin LC. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell 7: 1825-1834.
3. Babuke T, Tikkanen R. 2007. Dissecting the molecular function of reggie/flotillin proteins. Eur J Cell Biol 86: 525-532.
4. Balasubramanian N, Scott DW, Castle JD, Casanova JE, Schwartz MA. 2007. Arf6 and microtubules in adhesiondependent trafficking of lipid rafts. Nat Cell Biol 9: 11.
5. Barral DC, Garg S, Casalou C, Watts GF, Sandoval JL, Ramalho JS, Hsu VW, Brenner MB. 2012. Arl13b regulates endocytic recycling traffic. Proc Natl Acad Sci 109: 21354-21359.
6. Basquin C, Malarde V, Mellor P, Anderson DH, Meas-Yedid V, Olivo-Marin JC, Dautry-Varsat A, Sauvonnet N. 2013. The signalling factor PI3K is a specific regulator of the clathrin-independent dynamin-dependent endocytosis of IL-2 receptors. J Cell Sci 126: 1099-1108.
7. Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, Lo HP, Abankwa D, Luetterforst R, Fernandez-Rojo M, Breen MR, et al. 2009. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 185: 1259-1273.
8. Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, Wehland J, Rottner K. 2005. N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118: 3103-3115.
9. Bhagatji P, Leventis R, Comeau J, Refaei M, Silvius JR. 2009. Steric and not structure-specific factors dictate the endocytic mechanism of glycosylphosphatidylinositol-anchored proteins. J Cell Biol 186: 615-628.
10. Bohdanowicz M, Grinstein S. 2013. Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol Rev 93: 69-106.
11. Boucrot E, Howes MT, Kirchhausen T, Parton RG. 2011. Redistribution of caveolae during mitosis. J Cell Sci 124: 1965-1972.
12. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. 2001. Phosphatidylinositol 4, 5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 154: 1007-1017.
13. Burd C, Cullen PJ. 2014. Retromer: A master conductor of endosome sorting. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016774.
14. Cai B, Katafiasz D, Horejsi V, Naslavsky N. 2011. Pre-sorting endosomal transport of the GPI-anchored protein, CD59, is regulated by EHD1. Traffic 12: 102-120.
15. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS. 2002. Atubular EHD1- containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J 21: 2557-2567.
16. Cerezo A, Guadamillas MC, Goetz JG, Sanchez-Perales S, Klein E, Assoian RK, del Pozo MA. 2009. The absence of caveolin-1 increases proliferation and anchorage-independent growth by a Rac-dependent, Erk-independent mechanism. Mol Cell Biol 29: 5046-5059.
17. Chadda R, Howes MT, Plowman SJ, Hancock JF, Parton RG, Mayor S. 2007. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8: 702-717.
18. Chaudhry A, Das SR, Jameel S, George A, Bal V, Mayor S, Rath S. 2007. A two-pronged mechanism for HIV-1 Nefmediated endocytosis of immune costimulatory molecules CD80 and CD86. Cell Host Microbe 1: 37-49.
19. Cheng ZJ, Singh RD, Holicky EL, Wheatley CL, Marks DL, Pagano RE. 2010. Co-regulation of caveolar and Cdc42-dependent fluid phase endocytosis by phosphocaveolin- 1. J Biol Chem 285: 15119-15125.
20. Conner SD, Schmid SL. 2003. Regulated portals of entry into the cell. Nature 422: 37-44.
21. Cossart P, Helenius A. 2014. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol doi: 10.1101/ cshperspect.a016972.
22. Damke H, Baba T, Warnock DE, Schmid SL. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127: 915-934.
23. Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A. 2005. Clathrin- and caveolin-1-independent endocytosis: Entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168: 477-488.
24. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. 2003. Distinct endocytic pathways regulate TGF-b receptor signalling and turnover. Nat Cell Biol 5: 410-421.
25. Doherty GJ, McMahon HT. 2009. Mechanisms of endocytosis. Annu Rev Biochem 78: 857-902.
26. Doxsey SJ, Brodsky FM, Blank GS, Helenius A. 1987. Inhibition of endocytosis by anti-clathrin antibodies. Cell 50: 453-463.
27. Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, Santiago Y, Lee AH, Vo TD, Doyon Y, Miller JC, et al. 2011. Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13: 331-337.
28. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, et al. 2001. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 9: 9.
29. Egami Y, Fukuda M, Araki N. 2011. Rab35 regulates phagosome formation through recruitment of ACAP2 in macrophages during FcgR-mediated phagocytosis. J Cell Sci 124: 3557-3567.
30. Eyster CA, Higginson JD, Huebner R, Porat-Shliom N, Weigert R, Wu WW, Shen RF, Donaldson JG. 2009. Discovery of new cargo proteins that enter cells through clathrinindependent endocytosis. Traffic 10: 590-599.
31. Eyster CA, Cole NB, Petersen S, Viswanathan K, Fruh K, Donaldson JG. 2011. MARCH ubiquitin ligases alter the itinerary of clathrin-independent cargo from recycling to degradation. Mol Biol Cell 22: 3218-3230.
32. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE, Parton RG, van der Goot FG. 2002. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 21: 3989-4000.
33. Flannagan RS, Jaumouille V, Grinstein S. 2012. The cell biology of phagocytosis. Annu Rev Pathol 7: 61-98.
34. Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ. 2007. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17: 1151-1156.
35. Gaffen SL. 2001. Signaling domains of the interleukin 2 receptor. Cytokine 14: 63-77.
36. Galletta BJ, Cooper JA. 2009. Actin and endocytosis: Mechanisms and phylogeny. Curr Opin Cell Biol 21: 20-27.
37. Gauthier NC, Rossier OM, Mathur A, Hone JC, Sheetz MP. 2009. Plasma membrane area increases with spread area by exocytosis of a GPI-anchored protein compartment. Mol Biol Cell 20: 3261-3272.
38. Geli MI, Riezman H. 1996. Role of type I myosins in receptor- mediated endocytosis in yeast. Science 272: 533-535.
39. Gesbert F, Sauvonnet N, Dautry-Varsat A. 2004. Clathrinindependent endocytosis and signalling of interleukin 2 receptors IL-2R endocytosis and signalling. Curr Top Microbiol Immunol 286: 119-148.
40. Glebov OO, Bright NA, Nichols BJ. 2006. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8: 46-54.
41. Gong Q, Weide M, Huntsman C, Xu Z, Jan LY, Ma D. 2007. Identification and characterization of a new class of trafficking motifs for controlling clathrin-independent internalization and recycling. J Biol Chem 282: 13087-13097.
42. Gowrishankar K, Ghosh S, Saha SCR, Mayor S, Rao M. 2012. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149: 1353-1367.
43. Grant BD, Donaldson JG. 2009. Pathways and mechanisms of endocytic recycling.Nat RevMolCell Biol 10: 597-608.
44. Grant D, Unadkat S, Katzen A, Krishnan KS, Ramaswami M. 1998. Probable mechanisms underlying interallelic complementation and temperature-sensitivity of mutations at the shibire locus of Drosophila melanogaster. Genetics 149: 1019-1030.
45. Grassart A, Dujeancourt A, Lazarow PB, Dautry-Varsat A, Sauvonnet N. 2008. Clathrin-independent endocytosis used by the IL-2 receptor is regulated by Rac1, Pak1 and Pak2. EMBO Rep 9: 356-362.
46. Grassart A, Meas-Yedid V, Dufour A, Olivo-Marin JC, Dautry-Varsat A, Sauvonnet N. 2010. Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin- independent endocytosis. Traffic 11: 1079-1091.
47. Guha A, Sriram V, Krishnan KS, Mayor S. 2003. Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J Cell Sci 116: 3373-3386.
48. Gupta GD, Swetha MG, Kumari S, Lakshminarayan R, Dey G, Mayor S. 2009. Analysis of endocytic pathways in Drosophila cells reveals a conserved role for GBF1 in internalization via GEECs. PLoS ONE 4: e6768.
49. Hansen CG, Nichols BJ. 2010. Exploring the caves: Cavins, caveolins and caveolae. Trends Cell Biol 20: 177-186.
50. Hansen CG, Howard G, Nichols BJ. 2011. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 124: 2777-2785.
51. Hayer A, Stoeber M, Bissig C, Helenius A. 2010a. Biogenesis of caveolae: Stepwise assembly of large caveolin and cavin complexes. Traffic 11: 361-382.
52. Hayer A, Stoeber M, Ritz D, Engel S, Meyer HH, Helenius A. 2010b. Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 191: 615-629.
53. Hemar A, Lieb M, Subtil A, DiSanto JP, Dautry-Varsat A. 1994. Endocytosis of the b chain of interleukin-2 receptor requires neither interleukin-2 nor the g chain. Eur J Immunol 24: 1951-1955.
54. Hemar A, Subtil A, Lieb M, Morelon E, Hellio R, Dautry-Varsat A. 1995. Endocytosis of interleukin 2 receptors in human T lymphocytes: Distinct intracellular localization and fate of the receptor a, b, and g chains. J Cell Biol 129: 55-64.
55. Henley JR, Krueger EW, Oswald BJ, McNiven MA. 1998. Dynamin-mediated internalization of caveolae. J Cell Biol 141: 85-99.
56. Henne WM, Stenmark H, Emr SD. 2013. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol 5: a016766.
57. Hernandez-Deviez DJ, Howes MT, Laval SH, Bushby K, Hancock JF, Parton RG. 2008. Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J Biol Chem 283: 6476-6488.
58. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, et al. 2008. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132: 113-124.
59. Howes MT, Kirkham M, Riches J, Cortese K, Walser PJ, Simpson F, Hill MM, Jones A, Lundmark R, Lindsay MR, et al. 2010a. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol 190: 675-691.
60. Howes MT, Mayor S, Parton RG. 2010b. Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Curr Opin Cell Biol 22: 519-527.
61. Jiang X, Sorkin A. 2003. Epidermal growth factor receptor internalization through clathrin-coated pits requires Cbl RING finger and proline-rich domains but not receptor polyubiquitylation. Traffic 4: 529-543.
62. Johannes L, Mayor S. 2010. Induced domain formation in endocytic invagination, lipid sorting, and scission. Cell 142: 507-510.
63. Johannes L, Wunder C, Bassereau. 2014. Bending "on the rocks"-A cocktail of biophysical modules to build endoyctic pathways. Cold Spring Harb Perspect Biol 6: a016741.
64. Kaksonen M, Sun Y, Drubin DG. 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115: 475-487.
65. Kaksonen M, Toret CP, Drubin DG. 2005. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123: 305-320.
66. Kalia M, Kumari S, Chadda R, Hill MM, Parton RG, Mayor S. 2006. Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-30-kinasedependent machinery. Mol Biol Cell 17: 3689-3704.
67. Kirchhausen T, Owen D, Harrison SC, et al. 2014.Molecular Structure, Function and Dynamics of Clathrin-Mediated Membrane Traffic. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016725.
68. Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG. 2005. Ultrastructural identification of uncoated caveolin- independent early endocytic vehicles. J Cell Biol 168: 465-476.
69. Klumperman J, Raposo G. 2014. The complex ultrastructure of the endo-lysosome system. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016857.
70. Kobayashi H, Fukuda M. 2012. Rab35 regulates Arf6 activity through centaurin-b2 (ACAP2) during neurite outgrowth. J Cell Sci 125: 2235-2243.
71. Kouranti I, Sachse M, Arouche N, Goud B, Echard A. 2006. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16: 1719-1725.
72. Kukulski W, Schorb M, Kaksonen M, Briggs JA. 2012. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150: 508-520.
73. Kumari S, Mayor S. 2008. ARF1 is directly involved in dynamin- independent endocytosis. Nat Cell Biol 10: 30-41.
74. Kumari S, Borroni V, Chaudhry A, Chanda B, Massol R, Mayor S, Barrantes FJ. 2008. Nicotinic acetylcholine receptor is internalized via a Rac-dependent, dynaminindependent endocytic pathway. J Cell Biol 181: 1179-1193.
75. Kumari S, Mg S, Mayor S. 2010. Endocytosis unplugged: Multiple ways to enter the cell. Cell Res 20: 256-275.
76. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A. 2001. Interleukin 2 receptors and detergent- resistant membrane domains define a clathrinindependent endocytic pathway. Mol Cell 7: 661-671.
77. Liu J, Kaksonen M, Drubin DG, Oster G. 2006. Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci 103: 10277-10282.
78. Ludwig A, Howard G, Mendoza-Topaz C, Deerinck T, Mackey M, Sandin S, Ellisman MH, Nichols BJ. 2013. Molecularcomposition and ultrastructure of the caveolar coat complex. PLoS Biol 11: e1001640.
79. Lundmark R, Doherty GJ, Howes MT, Cortese K, Vallis Y, Parton RG, McMahon HT. 2008. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr Biol 18: 1802-1808.
80. Malan D, Elischer A, Hesse M, Wickstrom SA, Fleischmann BK, Bloch W. 2013. Deletion of integrin linked kinase in endothelial cells results in defective RTK signaling caused by caveolin 1 mislocalization. Development 140: 987-995.
81. Maldonado-Baez L, Cole NB, Kramer H, Donaldson JG. 2013a. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J Cell Biol 201: 233-247.
82. Maldonado-Baez L, Williamson C, Donaldson JG. 2013b. Clathrin-independent endocytosis: A cargo-centric view. Exp Cell Res 319: 2759-2769.
83. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR 2nd, Raleigh DR, Guan Y, Watson AJ, Montrose MH, et al. 2010. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126.
84. Mayor S. 2011. Need tension relief fast? Try caveolae. Cell 144: 323-324.
85. Mayor S, Pagano RE. 2007. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8: 603-612.
86. McIntosh DP, Schnitzer JE. 1999. Caveolae require intact VAMP for targeted transport in vascular endothelium. Am J Physiol 277: H2222-H2232.
87. McKenzie JE, Raisley B, Zhou X, Naslavsky N, Taguchi T, Caplan S, Sheff D. 2012. Retromer guides STxB and CD8- M6PR from early to recycling endosomes, EHD1 guides STxB from recycling endosome to Golgi. Traffic 13: 1140-1159.
88. Merrifield CJ, Kaksonen M. 2014. Endocytic accessory factors and regulation of clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol doi: 10.1101/cshper spect.a016733.
89. Miaczynska M, Pelkmans L, Zerial M. 2004. Not just a sink: Endosomes in control of signal transduction. Curr Opin Cell Biol 16: 400-406.
90. Montesano R, Roth J, Robert A, Orci L. 1982. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296: 651-653.
91. Moren B, Shah C, Howes MT, Schieber NL, McMahon HT, Parton RG, Daumke O, Lundmark R. 2012. EHD2 regulates caveolar dynamics via ATP-driven targeting and oligomerization. Mol Biol Cell 23: 1316-1329.
92. Moya M, Dautry-Varsat A, Goud B, Louvard D, Boquet P. 1985. Inhibition of coated pit formation in Hep2 cells blocks the cytotoxicity of diphtheria toxin but not that of ricin toxin. J Cell Biol 101: 548-559.
93. Munn AL, Silveira L, Elgort M, Payne GS. 1991. Viability of clathrin heavy-chain-deficient Saccharomyces cerevisiae is compromised by mutations at numerous loci: Implications for the suppression hypothesis. Mol Cell Biol 11: 3868-3878.
94. Munn AL, Stevenson BJ, Geli MI, Riezman H. 1995. end5, end6, and end7:Mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol Biol Cell 6: 1721-1742.
95. Muriel O, Echarri A, Hellriegel C, Pavon DM, Beccari L, Del Pozo MA. 2011. Phosphorylated filamin A regulates actin- linked caveolae dynamics. J Cell Sci 124: 2763-2776.
96. Naslavsky N, Caplan S. 2011. EHDproteins: Key conductors of endocytic transport. Trend Cell Biol 21: 122-131.
97. Naslavsky N, Weigert R, Donaldson JG. 2003. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 14: 417-431.
98. Naslavsky N, Weigert R, Donaldson JG. 2004. Characterization of a nonclathrin endocytic pathway:Membrane cargo and lipid requirements. Mol Biol Cell 15: 3542-3552.
99. Nishimura Y, Bereczky B, Yoshioka K, Taniguchi S, Itoh K. 2011. A novel role of Rho-kinase in the regulation of ligand-induced phosphorylated EGFR endocytosis via the early/late endocytic pathway in human fibrosarcoma cells. J Mol Histol 42: 427-442.
100. Ogata T, Ueyama T, Isodono K, Tagawa M, Takehara N, Kawashima T, Harada K, Takahashi T, Shioi T, Matsubara H, et al. 2008. MURC, a muscle-restricted coiled-coil protein that modulates the Rho/ROCK pathway, induces cardiac dysfunction and conduction disturbance. Mol Cell Biol 28: 3424-3436.
101. Oh P, McIntosh DP, Schnitzer JE. 1998. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141: 101-114.
102. Oh P, Borgstrom P, Witkiewicz H, Li Y, Borgstrom BJ, Chrastina A, Iwata K, Zinn KR, Baldwin R, Testa JE, et al. 2007. Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nature Biotechnol 25: 327-337.
103. Oh P, Horner T, Witkiewicz H, Schnitzer JE. 2012. Endothelin induces rapid, dynamin-mediated budding of endothelial caveolae rich in ET-B. J Biol Chem 287: 17353-17362.
104. Orlichenko L, Weller SG, Cao H, Krueger EW, Awoniyi M, Beznoussenko G, Buccione R, McNiven MA. 2009. Caveolae mediate growth factor-induced disassembly of adherens junctions to support tumor cell dissociation. Mol Biol Cell 20: 4140-4152.
105. Otto GP, Nichols BJ. 2011. The roles of flotillin microdomains- Endocytosis and beyond. J Cell Sci 124: 3933-3940.
106. Park DS, Woodman SE, Schubert W, Cohen AW, Frank PG, Chandra M, Shirani J, Razani B, Tang B, Jelicks LA, et al. 2002. Caveolin-1/3 double-knockout mice are viable, but lack both muscle and non-muscle caveolae, and develop a severe cardiomyopathic phenotype. Am J Pathol 160: 2207-2217.
107. Parton RG, Del Pozo MA. 2013. Caveolae as plasma membrane sensors, protectors, and organizers. Nat Rev Mol Cell Biol 14: 98-112.
108. Parton RG, Joggerst B, Simons K. 1994. Regulated internalization of caveolae. J Cell Biol 127: 1199-1215.
109. Payne GS. 1990. Genetic analysis of clathrin function in yeast. J Membr Biol 116: 93-105.
110. Pelkmans L, Zerial M. 2005. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436: 128-133.
111. Pelkmans L, Kartenbeck J, Helenius A. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular- transport pathway to the ER. Nat Cell Biol 3: 473-483.
112. Pelkmans L, Burli T, Zerial M, Helenius A. 2004. Caveolinstabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118: 767-780.
113. Piper RC, Lehner PJ. 2011. Endosomal transport via ubiquitination. Trend Cell Biol 21: 647-655.
114. Powelka AM, Sun J, Li J, Gao M, Shaw LM, Sonnenberg A, Hsu VW. 2004. Stimulation-dependent recycling of integrin b1 regulated by ARF6 and Rab11. Traffic 5: 20-36.
115. Puri C. 2009. Loss of myosin VI no insert isoform (NoI) induces a defect in clathrin-mediated endocytosis and leads to caveolar endocytosis of transferrin receptor. J Biol Chem 284: 34998-35014.
116. Pust S, Dyve AB, Torgersen ML, van Deurs B, Sandvig K. 2010. Interplay between toxin transport and flotillin localization. PLoS ONE 5: e8844.
117. Radhakrishna H, Donaldson JG. 1997. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 139: 49-61.
118. Riento K, Frick M, Schafer I, Nichols BJ. 2009. Endocytosis of flotillin-1 and flotillin-2 is regulated by Fyn kinase. J Cell Sci 122: 912-918.
119. Ritter TE, Fajardo O, Matsue H, Anderson RG, Lacey SW. 1995. Folate receptors targeted to clathrin-coated pits cannot regulate vitamin uptake. Proc Natl Acad Sci 92: 3824-3828.
120. Rocca A, Lamaze C, Subtil A, Dautry-Varsat A. 2001. Involvement of the ubiquitin/proteasome system in sorting of the interleukin 2 receptor b chain to late endocytic compartments. Mol Biol Cell 12: 1293-1301.
121. Romer W, Berland L, Chambon V, Gaus K, Windschiegl B, Tenza D, Aly MR, Fraisier V, Florent JC, Perrais D, et al. 2007. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450: 670-675.
122. Romer W, Pontani LL, Sorre B, Rentero C, Berland L, Chambon V, Lamaze C, Bassereau P, Sykes C, Gaus K, et al. 2010. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 140: 540-553.
123. Saavedra L, Mohamed A, Ma V, Kar S, de Chaves EP. 2007. Internalization of b-amyloid peptide by primary neurons in the absence of apolipoprotein E. J Biol Chem 282: 35722-35732.
124. Sabharanjak S, Mayor S. 2004. Folate receptor endocytosis and trafficking. Adv Drug Deliv Rev 56: 1099-1109.
125. Sabharanjak S, Sharma P, Parton RG, Mayor S. 2002. GPIanchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2: 411-423.
126. Sandvig K, van Deurs B. 1994. Endocytosiswithout clathrin. Trend Cell Biol 4: 275-277.
127. Sandvig K, Torgersen ML, Raa HA, van Deurs B. 2008. Clathrin-independent endocytosis: From nonexisting to an extreme degree of complexity. Histochem Cell Biol 129: 267-276.
128. Santy LC, Casanova JE. 2001. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J Cell Biol 154: 599-610.
129. Saslowsky DE, Cho JA, Chinnapen H, Massol RH, Chinnapen DJ, Wagner JS, De Luca HE, Kam W, Paw BH, Lencer WI. 2010. Intoxication of zebrafish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2. J Clin Invest 120: 4399-4409.
130. Sato M, Sato K, Liou W, Pant S, Harada A, Grant BD. 2008. Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J 27: 1183-1196.
131. Schnitzer JE, Liu J, Oh P. 1995. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J Biol Chem 270: 14399-14404.
132. Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S. 2011. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 124: 2032-2040.
133. Sharma P, Varma R, Sarasij RC, Ira, Gousset K, Krishnamoorthy G, Rao M, Mayor S. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-589.
134. Shi A, Liu O, Koenig S, Banerjee R, Chen CC, Eimer S, Grant BD. 2012. RAB-10-GTPase-mediated regulation of endosomal phosphatidylinositol-4, 5-bisphosphate. Proc Natl Acad Sci 109: E2306-E2315.
135. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci 102: 2760-2765.
136. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. 2008. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15: 209-219.
137. Sigismund S, Algisi V, Nappo G, Conte A, Pascolutti R, Cuomo A, Bonaldi T, Argenzio E, Verhoef LG, Maspero E, et al. 2013. Threshold-controlled ubiquitination of the EGFR directs receptor fate. EMBO J 32: 2140-2157.
138. Simionescu M, Gafencu A, Antohe F. 2002. Transcytosis of plasma macromolecules in endothelial cells: A cell biological survey. Microsc Res Tech 57: 269-288.
139. Sinha B, Koster D, Ruez R, Gonnord P, Bastiani M, Abankwa D, Stan RV, Butler-Browne G, Vedie B, Johannes L, et al. 2011. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144: 402-413.
140. Song J, Khachikian Z, Radhakrishna H, Donaldson JG. 1998. Localization of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J Cell Sci 111: 2257-2267.
141. Spoden G, Freitag K, Husmann M, Boller K, Sapp M, Lambert C, Florin L. 2008. Clathrin- and caveolin-independent entry of human papillomavirus type 16-Involvement of tetraspanin-enriched microdomains (TEMs). PLoS ONE 3: e3313.
142. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, Sherman MB, Geissler PL, Fletcher DA, Hayden CC. 2012. Membrane bending by protein-protein crowding. Nat Cell Biol 14: 944-949.
143. Stang E, Kartenbeck J, Parton RG. 1997. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol Biol Cell 8: 47-57.
144. Stoeber M, Stoeck IK, Hanni C, Bleck CK, Balistreri G, Helenius A. 2012. Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J 31: 2350-2364.
145. Subtil A, Hemar A, Dautry-Varsat A. 1994. Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J Cell Sci 107: 3461-3468.
146. Sverdlov M, Shinin V, Place AT, Castellon M, Minshall RD. 2009. Filamin A regulates caveolae internalization and trafficking in endothelial cells. Mol Biol Cell 20: 4531-4540.
147. Tagawa M, Ueyama T, Ogata T, Takehara N, Nakajima N, Isodono K, Asada S, Takahashi T, Matsubara H, Oh H. 2008. MURC, a muscle-restricted coiled-coil protein, is involved in the regulation of skeletal myogenesis. Am J Physiol Cell Physiol 295: C490-C498.
148. Tan PK, Davis NG, Sprague GF, Payne GS. 1993. Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast. J Cell Biol 123: 1707-1716.
149. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B. 2002. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13: 238-250.
150. Timpson P, Lynch DK, Schramek D, Walker F, Daly RJ. 2005. Cortactin overexpression inhibits ligand-induced downregulation of the epidermal growth factor receptor. Cancer Res 65: 3273-3280.
151. Toret CP, Drubin DG. 2006. The budding yeast endocytic pathway. J Cell Sci 119: 4585-4587.
152. Tran D, Carpentier JL, Sawano F, Gorden P, Orci L. 1987. Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc Natl Acad Sci 84: 7957-7961.
153. Way M, Parton RG. 1995. M-caveolin, a muscle-specific caveolin-related protein. FEBS Lett 376: 108-112.
154. Weigert R, Yeung AC, Li J, Donaldson JG. 2004. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol Biol Cell 15: 3758-3770.
155. Weinberg J, Drubin DG. 2012. Clathrin-mediated endocytosis in budding yeast. Trend Cell Biol 22: 1-13.
156. Wickstrom SA, Lange A, Hess MW, Polleux J, Spatz JP, Kruger M, Pfaller K, Lambacher A, Bloch W, Mann M, et al. 2010. Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev Cell 19: 574-588.
157. Zimmermann P, Tomatis D, Rosas M, Grootjans J, Leenaerts I, Degeest G, Reekmans G, Coomans C, David G. 2001. Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol Biol Cell 12: 339-350.