Building endocytic pits without clathrin

This article has been updated

Abstract

How endocytic pits are built in clathrin- and caveolin-independent endocytosis still remains poorly understood. Recent insight suggests that different forms of clathrin-independent endocytosis might involve the actin-driven focusing of membrane constituents, the lectin–glycosphingolipid-dependent construction of endocytic nanoenvironments, and Bin–Amphiphysin–Rvs (BAR) domain proteins serving as scaffolding modules. We discuss the need for different types of internalization processes in the context of diverse cellular functions, the existence of clathrin-independent mechanisms of cargo recruitment and membrane bending from a biological and physical perspective, and finally propose a generic scheme for the formation of clathrin-independent endocytic pits.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Mechanisms for physically bending membranes.
Figure 2: Clustering of membrane components as a consequence of active organization of short actin filaments.
Figure 3: Lectin-driven mechanisms for building endocytic pits.
Figure 4: The formation of a generic clathrin-independent endocytic pit.

Accession codes

Accessions

Protein Data Bank

Change history

  • 17 April 2015

    A note was added to page 9 of this Opinion to highlight a relevant study that was published while the proofs of this article were being finalized.

References

  1. 1

    Howes, M. T., Mayor, S. & Parton, R. G. Molecules, mechanisms, and cellular roles of clathrin-independent endocytosis. Curr. Opin. Cell Biol. 22, 519–527 (2010).

    CAS  Article  Google Scholar 

  2. 2

    Mayor, S. & Pagano, R. E. Pathways of clathrin-independent endocytosis. Nature Rev. Mol. Cell Biol. 8, 603–612 (2007).

    CAS  Article  Google Scholar 

  3. 3

    Johannes, L., Wunder, C. & Bassereau, P. Bending “on the rocks” — a cocktail of biophysical modules to build endocytic pathways. Cold Spring Harb. Perspect. Biol. 6, a016741 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Parton, R. G. & del Pozo, M. A. Caveolae as plasma membrane sensors, protectors and organizers. Nature Rev. Mol. Cell Biol. 14, 98–112 (2013).

    CAS  Article  Google Scholar 

  5. 5

    McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Rev. Mol. Cell Biol. 12, 517–533 (2011).

    CAS  Article  Google Scholar 

  6. 6

    Kirchhausen, T., Owen, D. & Harrison, S. C. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol. 6, a016725 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Lajoie, P. & Nabi, I. R. Lipid rafts, caveolae, and their endocytosis. Int. Rev. Cell. Mol. Biol. 282, 135–163 (2010).

    CAS  Article  Google Scholar 

  8. 8

    Moya, M., Dautry-Varsat, A., Goud, B., Louvard, D. & Boquet, P. 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 (1985).

    CAS  Article  Google Scholar 

  9. 9

    Sandvig, K., Olsnes, S., Petersen, O. W. & van Deurs, B. Acidification of the cytosol inhibits endocytosis from coated pits. J. Cell Biol. 105, 679–689 (1987).

    CAS  Article  Google Scholar 

  10. 10

    Sandvig, K. & van Deurs, B. Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis. J. Biol. Chem. 265, 6382–6388 (1990).

    CAS  PubMed  Google Scholar 

  11. 11

    Damke, H., Baba, T., van der Bliek, A. M. & Schmid, S. L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69–80 (1995).

    CAS  Article  Google Scholar 

  12. 12

    Guha, A., Sriram, V., Krishnan, K. S. & Mayor, S. Shibire mutations reveal distinct dynamin-independent and -dependent endocytic pathways in primary cultures of Drosophila hemocytes. J. Cell Sci. 116, 3373–3386 (2003).

    CAS  Article  Google Scholar 

  13. 13

    Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell 2, 411–423 (2002).

    CAS  Article  Google Scholar 

  14. 14

    Saint-Pol, A. et al. Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev. Cell 6, 525–538 (2004).

    CAS  Article  Google Scholar 

  15. 15

    Liu, Y. W., Surka, M. C., Schroeter, T., Lukiyanchuk, V. & Schmid, S. L. Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol. Biol. Cell 19, 5347–5359 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16

    Ferguson, S. M. et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell 17, 811–822 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17

    Stahlschmidt, W., Robertson, M. J., Robinson, P. J., McCluskey, A. & Haucke, V. Clathrin terminal domain-ligand interactions regulate sorting of mannose 6-phosphate receptors mediated by AP-1 and GGA adaptors. J. Biol. Chem. 289, 4906–4918 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18

    Bitsikas, V., Correa, I. R. Jr & Nichols, B. J. Clathrin-independent pathways do not contribute significantly to endocytic flux. eLife 3, e03970 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

    Kirkham, M. et al. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465–476 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20

    Howes, M. T. et al. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J. Cell Biol. 190, 675–691 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21

    Kumari, S. & Mayor, S. ARF1 is directly involved in dynamin-independent endocytosis. Nature Cell Biol. 10, 30–41 (2008).

    CAS  Article  Google Scholar 

  22. 22

    Lundmark, R. et al. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 18, 1802–1808 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23

    Doherty, G. J. et al. The endocytic protein GRAF1 is directed to cell-matrix adhesion sites and regulates cell spreading. Mol. Biol. Cell 22, 4380–4389 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24

    Kalia, M. et al. Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-3′-kinase-dependent machinery. Mol. Biol. Cell 17, 3689–3704 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Radhakrishna, H. & Donaldson, J. G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49–61 (1997).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26

    Naslavsky, N., Weigert, R. & Donaldson, J. G. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol. Biol. Cell 14, 417–431 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27

    Eyster, C. A. et al. Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 10, 590–599 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28

    Eyster, C. A. et al. MARCH ubiquitin ligases alter the itinerary of clathrin-independent cargo from recycling to degradation. Mol. Biol. Cell 22, 3218–3230 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29

    Maldonado-Baez, L., Cole, N. B., Kramer, H. & Donaldson, J. G. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell Biol. 201, 233–247 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30

    Sigismund, S. et al. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209–219 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Lamaze, C. et al. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7, 661–671 (2001).

    CAS  Article  Google Scholar 

  32. 32

    Watanabe, S. et al. Clathrin regenerates synaptic vesicles from endosomes. Nature 515, 228–233 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33

    Mayor, S., Parton, R. G. & Donaldson, J. G. Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol. 6, a016758 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Chaudhary, N. et al. Endocytic crosstalk: cavins, caveolins, and caveolae regulate clathrin-independent endocytosis. PLoS Biol. 12, e1001832 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 35

    Dey, G. et al. Exploiting cell-to-cell variability to detect cellular perturbations. PLoS ONE 9, e90540 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    Kumari, S. Dynamin Independent Endocytosis: Molecular Mechanisms and Membrane Dynamics. Thesis, Natl Centre Biol. Sci., Tata Institute Fundam. Res. (2009).

  37. 37

    Römer, W. et al. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 140, 540–553 (2010).

    Article  CAS  Google Scholar 

  38. 38

    Gupta, G. D. et al. Population distribution analyses reveal a hierarchy of molecular players underlying parallel endocytic pathways. PLoS ONE 9, e100554 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Liberali, P., Snijder, B. & Pelkmans, L. A hierarchical map of regulatory genetic interactions in membrane trafficking. Cell 157, 1473–1487 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40

    Boucrot, E. et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517, 460–465 (2015)

    CAS  Article  Google Scholar 

  41. 41

    Sinha, B. et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144, 402–413 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42

    Helfrich, W. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch C 28, 693–703 (1973).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43

    Leduc, C., Campas, O., Joanny, J. F., Prost, J. & Bassereau, P. Mechanism of membrane nanotube formation by molecular motors. Biochim. Biophys. Acta 1798, 1418–1426 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44

    Soldati, T. & Schliwa, M. Powering membrane traffic in endocytosis and recycling. Nature Rev. Mol. Cell Biol. 7, 897–908 (2006).

    CAS  Article  Google Scholar 

  45. 45

    Almeida, C. G. et al. Myosin 1b promotes the formation of post-Golgi carriers by regulating actin assembly and membrane remodelling at the trans-Golgi network. Nature Cell Biol. 13, 779–789 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46

    Leduc, C. et al. Cooperative extraction of membrane nanotubes by molecular motors. Proc. Natl Acad. Sci. USA 101, 17096–17101 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 47

    Shaklee, P. M. et al. Bidirectional membrane tube dynamics driven by nonprocessive motors. Proc. Natl Acad. Sci. USA 105, 7993–7997 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48

    Yamada, A. et al. Catch-bond behaviour facilitates membrane tubulation by non-processive myosin 1b. Nature Commun. 5, 3624 (2014).

    Article  CAS  Google Scholar 

  49. 49

    Liu, J., Kaksonen, M., Drubin, D. G. & Oster, G. Endocytic vesicle scission by lipid phase boundary forces. Proc. Natl Acad. Sci. USA 103, 10277–10282 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50

    Kukulski, W., Schorb, M., Kaksonen, M. & Briggs, J. A. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150, 508–520 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51

    Idrissi, F. Z., Blasco, A., Espinal, A. & Geli, M. I. Ultrastructural dynamics of proteins involved in endocytic budding. Proc. Natl Acad. Sci. USA 109, E2587–E2594 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52

    Lipowsky, R. Coupling of bending and stretching deformations in vesicle membranes. Adv. Colloid Interface Sci. 208, 14–24 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53

    Julicher, F. & Lipowsky, R. Domain induced budding of vesicles. Phys. Rev. Lett. 70, 2964–2967 (1993).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54

    Sens, P., Johannes, L. & Bassereau, P. Biophysical view on protein-induced membrane deformations in endocytosis. Curr. Opin. Cell Biol. 20, 476–482 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 55

    Semrau, S. & Schmidt, T. Membrane heterogeneity — from lipid domains to curvature effects. Soft Matter 5, 3174–3186 (2009).

    CAS  Article  Google Scholar 

  56. 56

    Veatch, S. L. et al. Critical fluctuations in plasma membrane vesicles. ACS Chem. Biol. 3, 287–293 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. 57

    Leibler, S. Curvature instability in membranes. J. Phys. 47, 507–516 (1986).

    CAS  Article  Google Scholar 

  58. 58

    Campelo, F., McMahon, H. T. & Kozlov, M. M. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95, 2325–2339 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 59

    Blood, P. D., Swenson, R. D. & Voth, G. A. Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations. Biophys. J. 95, 1866–1876 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60

    Arkhipov, A., Yin, Y. & Schulten, K. Four-scale description of membrane sculpting by BAR domains. Biophys. J. 95, 2806–2821 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. 61

    Callan-Jones, A. & Bassereau, P. Curvature-driven membrane lipid and protein distribution. Curr. Opin. Solid St. M. 17, 143–150 (2013).

    CAS  Article  Google Scholar 

  62. 62

    Bhatia, V. K., Hatzakis, N. S. & Stamou, D. A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins. Semin. Cell Dev. Biol. 21, 381–390 (2010).

    CAS  Article  Google Scholar 

  63. 63

    Sorre, B. et al. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl Acad. Sci. USA 109, 173–178 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. 64

    Simunovic, M., Srivastava, A. & Voth, G. A. Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. Proc. Natl Acad. Sci. USA 110, 20396–20401 (2013).

    CAS  Article  Google Scholar 

  65. 65

    Rao, M. & Mayor, S. Active organization of membrane constituents in living cells. Curr. Opin. Cell Biol. 29, 126–132 (2014).

    CAS  Article  Google Scholar 

  66. 66

    Maitra, A., Srivastava, P., Rao, M. & Ramaswamy, S. Activating membranes. Phys. Rev. Lett. 112, 258101 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 67

    Gowrishankar, K. et al. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149, 1353–1367 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. 68

    Chen, B. et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156, 195–207 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. 69

    Grassart, A. et al. Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin-independent endocytosis. Traffic 11, 1079–1091 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. 70

    Kumari, S., Mg, S. & Mayor, S. Endocytosis unplugged: multiple ways to enter the cell. Cell. Res. 20, 256–275 (2010).

    CAS  Article  Google Scholar 

  71. 71

    Liu, J., Sun, Y., Drubin, D. G. & Oster, G. F. The mechanochemistry of endocytosis. PLoS Biol. 7, e1000204 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Montesano, R., Roth, J., Robert, A. & Orci, L. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296, 651–653 (1982).

    CAS  Article  Google Scholar 

  73. 73

    Torgersen, M. L., Skretting, G., van Deurs, B. & Sandvig, K. Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114, 3737–3747 (2001).

    CAS  PubMed  Google Scholar 

  74. 74

    Sandvig, K., Olsnes, S., Brown, J. E., Petersen, O. W. & van Deurs, B. Endocytosis from coated pits of Shiga toxin: a glycolipid-binding protein from Shigella dysenteriae 1. J. Cell Biol. 108, 1331–1343 (1989).

    CAS  Article  Google Scholar 

  75. 75

    Lauvrak, S. U. et al. Shiga toxin regulates its entry in a Syk-dependent manner. Mol. Biol. Cell 17, 1096–1109 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. 76

    Renard, H.-F. et al. Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature 517, 493–496 (2015).

    CAS  Article  Google Scholar 

  77. 77

    Römer, W. et al. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature 450, 670–675 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. 78

    Solovyeva, V., Johannes, L. & Simonsen, A. C. Shiga toxin induces membrane reorganization and formation of long range lipid order. Soft Matter 11, 186–192 (2014).

    Article  Google Scholar 

  79. 79

    Johannes, L. & Mayor, S. Induced domain formation in endocytic invagination, lipid sorting, and scission. Cell 142, 507–510 (2010).

    CAS  Article  Google Scholar 

  80. 80

    Ravindran, M. S., Tanner, L. B. & Wenk, M. R. Sialic acid linkage in glycosphingolipids is a molecular correlate for trafficking and delivery of extracellular cargo. Traffic 14, 1182–1191 (2013).

    CAS  PubMed  Google Scholar 

  81. 81

    Neu, U., Woellner, K., Gauglitz, G. & Stehle, T. Structural basis of GM1 ganglioside recognition by simian virus 40. Proc. Natl Acad. Sci. USA 105, 5219–5224 (2008).

    CAS  Article  Google Scholar 

  82. 82

    Ling, H. et al. Structure of Shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry 37, 1777–1788 (1998).

    CAS  Article  Google Scholar 

  83. 83

    Zhang, R. G. et al. The three-dimensional crystal structure of cholera toxin. J. Mol. Biol. 251, 563–573 (1995).

    CAS  Article  Google Scholar 

  84. 84

    Ewers, H. et al. GM1 structure determines SV40-induced membrane invagination and infection. Nature Cell Biol. 12, 11–18 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  85. 85

    Lakshminarayan, R. et al. Galectin-3 drives glycosphingolipid-dependent biogenesis of clathrin-independent carriers. Nature Cell Biol. 16, 595–606 (2014).

    CAS  Article  Google Scholar 

  86. 86

    Furtak, V., Hatcher, F. & Ochieng, J. Galectin-3 mediates the endocytosis of β-1 integrins by breast carcinoma cells. Biochem. Biophys. Res. Commun. 289, 845–850 (2001).

    CAS  Article  Google Scholar 

  87. 87

    Partridge, E. A. et al. Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306, 120–124 (2004).

    CAS  Article  Google Scholar 

  88. 88

    Gao, X. et al. The two endocytic pathways mediated by the carbohydrate recognition domain and regulated by the collagen-like domain of galectin-3 in vascular endothelial cells. PLoS ONE 7, e52430 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. 89

    Lepur, A. et al. Galectin-3 endocytosis by carbohydrate independent and dependent pathways in different macrophage like cell types. Biochim. Biophys. Acta 1820, 804–818 (2012).

    CAS  Article  Google Scholar 

  90. 90

    Iurisci, I. et al. Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin. Cancer Res. 6, 1389–1393 (2000).

    CAS  PubMed  Google Scholar 

  91. 91

    Christenson, R. H. et al. Multi-center determination of galectin-3 assay performance characteristics: anatomy of a novel assay for use in heart failure. Clin. Biochem. 43, 683–690 (2010).

    CAS  Article  Google Scholar 

  92. 92

    Hirabayashi, J. et al. Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572, 232–254 (2002).

    CAS  Article  Google Scholar 

  93. 93

    Collins, P. M., Bum-Erdene, K., Yu, X. & Blanchard, H. Galectin-3 interactions with glycosphingolipids. J. Mol. Biol. 426, 1439–1451 (2014).

    CAS  Article  Google Scholar 

  94. 94

    Lepur, A., Salomonsson, E., Nilsson, U. J. & Leffler, H. Ligand induced galectin-3 self-association. J. Biol. Chem. 287, 21751–21756 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  95. 95

    Delacour, D. et al. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J. Cell Biol. 169, 491–501 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  96. 96

    Mishra, R., Grzybek, M., Niki, T., Hirashima, M. & Simons, K. Galectin-9 trafficking regulates apical-basal polarity in Madin–Darby canine kidney epithelial cells. Proc. Natl Acad. Sci. USA 107, 17633–17638 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  97. 97

    Mim, C. & Unger, V. M. Membrane curvature and its generation by BAR proteins. Trends Biochem. Sci. 37, 526–533 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  98. 98

    Kozlov, M. M. et al. Mechanisms shaping cell membranes. Curr. Opin. Cell Biol. 29, 53–60 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. 99

    Frost, A., Unger, V. M. & De Camilli, P. The BAR domain superfamily: membrane-molding macromolecules. Cell 137, 191–196 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  100. 100

    Daumke, O., Roux, A. & Haucke, V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell 156, 882–892 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  101. 101

    Henne, W. M. et al. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281–1284 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  102. 102

    Umasankar, P. K. et al. Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning. Nature Cell Biol. 14, 488–501 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  103. 103

    Cocucci, E., Aguet, F., Boulant, S. & Kirchhausen, T. The first five seconds in the life of a clathrin-coated pit. Cell 150, 495–507 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  104. 104

    Tang, Y. et al. Identification of the endophilins (SH3p4/p8/p13) as novel binding partners for the β1-adrenergic receptor. Proc. Natl Acad. Sci. USA 96, 12559–12564 (1999).

    CAS  Article  Google Scholar 

  105. 105

    Gallop, J. L. et al. Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25, 2898–2910 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. 106

    Allain, J. M., Storm, C., Roux, A., Ben Amar, M. & Joanny, J. F. Fission of a multiphase membrane tube. Phys. Rev. Lett. 93, 158104 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. 107

    Milosevic, I. et al. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72, 587–601 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. 108

    Gad, H. et al. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301–312 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  109. 109

    Llobet, A. et al. Endophilin drives the fast mode of vesicle retrieval in a ribbon synapse. J. Neurosci. 31, 8512–8519 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  110. 110

    Kononenko, N. L. et al. Clathrin/AP-2 mediate synaptic vesicle reformation from endosome-like vacuoles but are not essential for membrane retrieval at central synapses. Neuron 82, 981–988 (2014).

    CAS  Article  Google Scholar 

  111. 111

    Hansen, C. G. & Nichols, B. J. Molecular mechanisms of clathrin-independent endocytosis. J. Cell Sci. 122, 1713–1721 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  112. 112

    Sorkin, A. Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16, 392–399 (2004).

    CAS  Article  Google Scholar 

  113. 113

    Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305–320 (2005).

    CAS  Article  Google Scholar 

  114. 114

    Hinrichsen, L., Harborth, J., Andrees, L., Weber, K. & Ungewickell, E. J. Effect of clathrin heavy chain- and α-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J. Biol. Chem. 278, 45160–45170 (2003).

    CAS  Article  Google Scholar 

  115. 115

    Montagnac, G. et al. αTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature 502, 567–570 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  116. 116

    Mim, C. et al. Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137–145 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  117. 117

    Shalom-Feuerstein, R. et al. K-ras nanoclustering is subverted by overexpression of the scaffold protein galectin-3. Cancer Res. 68, 6608–6616 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  118. 118

    Zhao, H. et al. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4, 1213–1223 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  119. 119

    Doherty, G. J. & McMahon, H. T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857–902 (2009).

    CAS  Article  Google Scholar 

  120. 120

    Shvets, E., Ludwig, A. & Nichols, B. J. News from the caves: update on the structure and function of caveolae. Curr. Opin. Cell Biol. 29, 99–106 (2014).

    CAS  Article  Google Scholar 

  121. 121

    Hansen, C. G. & Nichols, B. J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol. 20, 177–186 (2010).

    CAS  Article  Google Scholar 

  122. 122

    Ariotti, N. & Parton, R. G. SnapShot: caveolae, caveolins, and cavins. Cell 154, 704–704.e1 (2013).

    CAS  Article  Google Scholar 

  123. 123

    Boucrot, E., Howes, M. T., Kirchhausen, T. & Parton, R. G. Redistribution of caveolae during mitosis. J. Cell Sci. 124, 1965–1972 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  124. 124

    Stoeber, M. et al. Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J. 31, 2350–2364 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  125. 125

    Henley, J. R., Krueger, E. W., Oswald, B. J. & McNiven, M. A. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141, 85–99 (1998).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  126. 126

    Moren, B. et al. EHD2 regulates caveolar dynamics via ATP-driven targeting and oligomerization. Mol. Biol. Cell 23, 1316–1329 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  127. 127

    Oh, P., McIntosh, D. P. & Schnitzer, J. E. 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 (1998).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  128. 128

    Pelkmans, L., Burli, T., Zerial, M. & Helenius, A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767–780 (2004).

    CAS  Article  Google Scholar 

  129. 129

    Safouane, M. et al. Lipid cosorting mediated by Shiga toxin induced tubulation. Traffic 11, 1519–1529 (2010).

    CAS  Article  Google Scholar 

  130. 130

    Day, C. A. et al. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic http://dx.doi.org/10.1111/tra.12269 (2015).

Download references

Acknowledgements

The help of J. Ménétrey is acknowledged for the overlay in Figure 3b. L.J. is funded by grants from the European Community's Framework Programme under grant agreement numbers TRANSPOL-264399 and H2020-MSCA-ITN-2014, Agence Nationale pour la Recherche (ANR-11 BSV2 014 03, ANR-14-CE14-0002-02 and ANR-14-CE16-0004-03), Human Frontier Science Program (HFSP) grant RGP0029-2014, European Research Council advanced grant (project 340485) and INCa programme PLBIO11-022-IDF-JOHANNES. R.G.P. is funded by grants and fellowships from the National Health and Medical Research Council, Australia, and grants from the Australian Research Council. S.M. is supported by a JC Bose fellowship from the Department of Science and Technology and grants from HFSP RGP0027/2012 and a Centre of Excellence (CoE) grant from the Department of Biotechnology, Goverment of India. P.B. is funded by a European Research Concil advanced grant (project 339847) and by the Agence Nationale de la Recherche (ANR-11 BSV2 014 03, ANR-14-CE09-0003-03). The Johannes and Bassereau teams are members of Labex CelTisPhyBio (11-LBX-0038) and Idex Paris Sciences et Lettres (ANR-10-IDEX-0001-02 PSL). The facilities as well as scientific and technical assistance from staff in the PICT-IBiSA/Nikon Imaging Centre at Institut Curie-Centre National de la Recherche Scientifique (CNRS) and the France-BioImaging intrastructure (ANR-10-INSB-04) are acknowledged.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Ludger Johannes or Robert G. Parton or Patricia Bassereau or Satyajit Mayor.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Supplementary information

Supplementary information S1 (table)

Approaches for assessing forms of endocytosis (PDF 145 kb)

Supplementary information S2 (table)

Overview of endocytic processes (PDF 118 kb)

Related links

Related links

DATABASES

Protein Data Bank

1BOS

1FGB

3BWR

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Johannes, L., Parton, R., Bassereau, P. et al. Building endocytic pits without clathrin. Nat Rev Mol Cell Biol 16, 311–321 (2015). https://doi.org/10.1038/nrm3968

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing