CoChat
Sign Up
Cited by 614Cellular transport and secretionCaveolin-1 and cellular processesAutophagy in Disease and Therapy

Regulation of Clathrin-Mediated Endocytosis

Open access
Mettlen, Marcel, Chen, Ping-Hung, Srinivasan, Saipraveen, Danuser, Gaudenz, Schmid, Sandra L.·2018·Annual Review of Biochemistry
DOI 10.1146/annurev-biochem-062917-012644PMC PMC6383209
Open this paper in CoChat — free accountOpen PDF

Abstract

Clathrin-mediated endocytosis (CME) is the major endocytic pathway in mammalian cells. It is responsible for the uptake of transmembrane receptors and transporters, for remodeling plasma membrane composition in response to environmental changes, and for regulating cell surface signaling. CME occurs via the assembly and maturation of clathrin-coated pits that concentrate cargo as they invaginate and pinch off to form clathrin-coated vesicles. In addition to the major coat proteins, clathrin triskelia and adaptor protein complexes, CME requires a myriad of endocytic accessory proteins and phosphatidylinositol lipids. CME is regulated at multiple steps—initiation, cargo selection, maturation, and fission—and is monitored by an endocytic checkpoint that induces disassembly of defective pits. Regulation occurs via posttranslational modifications, allosteric conformational changes, and isoform and splice-variant differences among components of the CME machinery, including the GTPase dynamin. This review summarizes recent findings on the regulation of CME and the evolution of this complex process.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1146/annurev-biochem-062917-012644

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

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?

  • PI(4,5)P2 recruits dynamin to the plasma membrane where it assembles at the neck of the budding vesicle and mediates fusion of the non-cytosolic leaflets.

    “PI(4,5)P2 also plays a crucial role in the recruitment of dynamin to the plasma membrane where it assembles at the neck of the budding vesicle and mediates fusion of the non-cytosolic leaflets of the membrane [99].”

    From Phosphatidylinositol(4,5)bisphosphate: diverse functions at the plasma membrane (2020) · cites this paper as [99]

    The 'Dynamin: A Key Regulator of CME' section says dynamin assembles around the neck of deeply invaginated clathrin-coated pits and catalyzes membrane fission. 'Regulating CCP Growth and Maturation' links PI(4,5)P2 to a neck-localized SNX9 pathway, but does not establish that PI(4,5)P2 directly recruits dynamin. The passages do not describe dynamin mediating fusion of the non-cytosolic leaflets. Page numbers were not available in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Surface levels of membrane proteins are determined by the dynamic balance of exocytosis-mediated delivery and endocytosis-dependent retrieval.

    “The surface level of a protein is determined by the dynamic balance of its delivery to the plasma membrane through exocytic pathways (including recycling exocytosis) and removal from the plasma membrane by endocytic pathways (4–6).”

    From Regulation of cargo exocytosis by a Reps1-Ralbp1-RalA module (2023) · cites this paper as [6]

    The Introduction (page not available) says clathrin-mediated endocytosis takes up surface receptors and regulates the surface abundance of transmembrane transporters. It does not address exocytic delivery, including recycling exocytosis, or state that surface levels reflect a balance between delivery and removal. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Internalisation of nutrients, cargo-bound receptors and ligand-bound signalling receptors occurs by clathrin-mediated endocytosis, which requires PI(4,5)P2.

    “Internalisation of nutrients, cargo-bound receptors and ligand-bound signalling receptors takes place by clathrin-mediated endocytosis which requires PI(4,5)P2 [99].”

    From Phosphatidylinositol(4,5)bisphosphate: diverse functions at the plasma membrane (2020) · cites this paper as [99]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 144

  1. [1]Conner SD, Schmid SL. 2002 Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell Biol 156: 921– 29 11877461 PMC2173317
  2. [2]Robinson MS. 2015 Forty years of clathrin-coated vesicles. Traffic 16: 1210– 38 26403691
  3. [3]Schmid EM, McMahon HT. 2007 Integrating molecular and network biology to decode endocytosis. Nature 448: 883– 88 17713526
  4. [4]Antonny B, Burd C, De Camilli P, Chen E, Daumke O, 2016 Membrane fission by dynamin: what we know and what we need to know. EMBO J. 35: 2270– 84 27670760 PMC5090216
  5. [5]Morlot S, Roux A. 2013 Mechanics of dynamin-mediated membrane fission. Annu. Rev. Biophys 42: 629– 49 23541160 PMC4289195
  6. [6]Schmid SL, Frolov VA. 2011 Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol 27: 79– 105 21599493
  7. [7]Gaidarov I, Santini F, Warren RA, Keen JH. 1999 Spatial control of coated pit dynamics in living cells. Nat. Cell Biol 1: 1– 7 10559856
  8. [8]Merrifield CJ, Feldman ME, Wan L, Almers W. 2002 Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol 4: 691– 98 12198492
  9. [9]Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, 2004 Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591– 605 15339664
  10. [10]Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H, 2009 Cargo and dynamin regulate clathrin-coated pit maturation. PLOS Biol. 7: e57 19296720 PMC2656549
  11. [11]Taylor MJ, Perrais D, Merrifield CJ. 2011 A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLOS Biol. 9: e1000604 21445324 PMC3062526
  12. [12]Maxfield FR, McGraw TE. 2004 Endocytic recycling. Nat. Rev. Mol. Cell Biol 5: 121– 32 15040445
  13. [13]Burston HE, Maldonado-Baez L, Davey M, Montpetit B, Schluter C, 2009 Regulators of yeast endocytosis identified by systematic quantitative analysis. J. Cell Biol 185: 1097– 110 19506040 PMC2711619
  14. [15]Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T. 2011 Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol 13: 1124– 31 21841790 PMC3167020
  15. [16]Kural C, Akatay AA, Gaudin R, Chen BC, Legant WR, 2015 Asymmetric formation of coated pits on dorsal and ventral surfaces at the leading edges of motile cells and on protrusions of immobile cells. Mol. Biol. Cell 26: 2044– 53 25851602 PMC4472015
  16. [17]Saffarian S, Kirchhausen T. 2008 Differential evanescence nanometry: live-cell fluorescence measurements with 10-nm axial resolution on the plasma membrane. Biophys. J 94: 2333– 42 17993495 PMC2257884
  17. [18]Keyel PA, Watkins SC, Traub LM. 2004 Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy. J. Biol. Chem 279: 13190– 204 14722064
  18. [19]Mattheyses AL, Atkinson CE, Simon SM. 2011 Imaging single endocytic events reveals diversity in clathrin, dynamin and vesicle dynamics. Traffic 12: 1394– 406 21689254 PMC3245319
  19. [21]Rappoport JZ, Simon SM. 2003 Real-time analysis of clathrin-mediated endocytosis during cell migration. J. Cell Sci. 116: 847– 55 12571282
  20. [22]Grassart A, Cheng AT, Hong SH, Zhang F, Zenzer N, 2014 Actin and dynamin2 dynamics and interplay during clathrin-mediated endocytosis. J. Cell Biol 205: 721– 35 24891602 PMC4050722
  21. [23]Rappoport JZ, Taha BW, Lemeer S, Benmerah A, Simon SM. 2003 The AP-2 complex is excluded from the dynamic population of plasma membrane-associated clathrin. J. Biol. Chem 278: 47357– 60 14530274
  22. [24]Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, 2008 Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5: 695– 702 18641657 PMC2747604
  23. [25]Aguet F, Antonescu CN, Mettlen M, Schmid SL, Danuser G. 2013 Advances in analysis of low signal-to-noise images link dynamin and AP2 to the functions of an endocytic checkpoint. Dev. Cell 26: 279– 91 23891661 PMC3939604
  24. [26]Lampe M, Vassilopoulos S, Merrifield C. 2016 Clathrin coated pits, plaques and adhesion. J. Struct. Biol. 196: 48– 56 27431447
  25. [27]Mettlen M, Stoeber M, Loerke D, Antonescu CN, Danuser G, Schmid SL. 2009 Endocytic accessory proteins are functionally distinguished by their differential effects on the maturation of clathrin-coated pits. Mol. Biol. Cell 20: 3251– 60 19458185 PMC2710825
  26. [28]Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, 2011 Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat. Cell Biol 13: 331– 37 21297641 PMC4113319
  27. [29]Hong SH, Cortesio CL, Drubin DG. 2015 Machine-learning-based analysis in genome-edited cells reveals the efficiency of clathrin-mediated endocytosis. Cell Rep. 12: 2121– 30 26387943 PMC4610353
  28. [30]Mettlen M, Danuser G. 2014 Imaging and modeling the dynamics of clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol 6: a017038 25167858 PMC4292148
  29. [31]Saffarian S, Cocucci E, Kirchhausen T. 2009 Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLOS Biol. 7: e1000191 19809571 PMC2731173
  30. [32]Batchelder EM, Yarar D. 2010 Differential requirements for clathrin-dependent endocytosis at sites of cell-substrate adhesion. Mol. Biol. Cell 21: 3070– 79 20631253 PMC2929999
  31. [33]Maupin P, Pollard TD. 1983 Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. J. Cell Biol 96: 51– 62 6186673 PMC2112254
  32. [34]Elkhatib N, Bresteau E, Baschieri F, Rioja AL, van Niel G, 2017 Tubular clathrin/AP-2 lattices pinch collagen fibers to support 3D cell migration. Science 356: eaal4713 28619886
  33. [35]Grove J, Metcalf DJ, Knight AE, Wavre-Shapton ST, Sun T, 2014 Flat clathrin lattices: stable features of the plasma membrane. Mol. Biol. Cell 25: 3581– 94 25165141 PMC4230618
  34. [36]Cureton DK, Massol RH, Whelan SP, Kirchhausen T. 2010 The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLOS Pathog. 6: e1001127 20941355 PMC2947997
  35. [37]Skruzny M, Brach T, Ciuffa R, Rybina S, Wachsmuth M, Kaksonen M. 2012 Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. PNAS 109: E2533– 42 22927393 PMC3458359
  36. [38]Traub LM. 2009 Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol 10: 583– 96 19696796
  37. [39]Bonifacino JS, Traub LM. 2003 Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem 72: 395– 447 12651740
  38. [40]Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, 1995 Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269: 1872– 75 7569928
  39. [41]Maurer ME, Cooper JA. 2006 The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J. Cell Sci 119: 4235– 46 16984970
  40. [42]Garuti R, Jones C, Li WP, Michaely P, Herz J, 2005 The modular adaptor protein autosomal recessive hypercholesterolemia (ARH) promotes low density lipoprotein receptor clustering into clathrin-coated pits. J. Biol. Chem 280: 40996– 1004 16179341
  41. [43]Hopkins CR, Miller K, Beardmore JM. 1985 Receptor-mediated endocytosis of transferrin and epidermal growth factor receptors: a comparison of constitutive and ligand-induced uptake. J. Cell Sci. Suppl 3: 173– 86 3011821
  42. [44]Trowbridge IS, Collawn JF, Hopkins CR. 1993 Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol 9: 129– 61 8280459
  43. [45]Milano SK, Pace HC, Kim YM, Brenner C, Benovic JL. 2002 Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis. Biochemistry 41: 3321– 28 11876640
  44. [46]Henry AG, Hislop JN, Grove J, Thorn K, Marsh M, von Zastrow M. 2012 Regulation of endocytic clathrin dynamics by cargo ubiquitination. Dev. Cell 23: 519– 32 22940114 PMC3470869
  45. [47]Miller WE, Lefkowitz RJ. 2001 Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr. Opin. Cell Biol 13: 139– 45 11248546
  46. [48]Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, 2002 A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J. 21: 303– 13 11823423 PMC125825
  47. [49]Bertelsen V, Sak MM, Breen K, Rodland MS, Johannessen LE, 2011 A chimeric pre-ubiquitinated EGF receptor is constitutively endocytosed in a clathrin-dependent, but kinase-independent manner. Traffic 12: 507– 20 21226813
  48. [50]de Melker AA, van der Horst G, Borst J. 2004 c-Cbl directs EGF receptors into an endocytic pathway that involves the ubiquitin-interacting motif of Eps15. J. Cell Sci 117: 5001– 12 15383614
  49. [51]Regan-Klapisz E, Sorokina I, Voortman J, de Keizer P, Roovers RC, 2005 Ubiquilin recruits Eps15 into ubiquitin-rich cytoplasmic aggregates via a UIM-UBL interaction. J. Cell Sci 118: 4437– 50 16159959
  50. [52]Confalonieri S, Salcini AE, Puri C, Tacchetti C, Di Fiore PP. 2000 Tyrosine phosphorylation of Eps15 is required for ligand-regulated, but not constitutive, endocytosis. J. Cell Biol 150: 905– 12 10953014 PMC2175269
  51. [53]Pitcher C, Honing S, Fingerhut A, Bowers K, Marsh M. 1999 Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 10: 677– 91 10069811 PMC25195
  52. [54]Miettinen HM, Matter K, Hunziker W, Rose JK, Mellman I. 1992 Fc receptor endocytosis is controlled by a cytoplasmic domain determinant that actively prevents coated pit localization. J. Cell Biol 116: 875– 88 1734021 PMC2289334
  53. [55]Liu AP, Aguet F, Danuser G, Schmid SL. 2010 Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J. Cell Biol 191: 1381– 93 21187331 PMC3010081
  54. [56]Kadlecova Z, Spielman SJ, Loerke D, Mohanakrishnan A, Reed DK, Schmid SL. 2017 Regulation of clathrin-mediated endocytosis by hierarchical allosteric activation of AP2. J. Cell Biol 216: 167– 79 28003333 PMC5223608
  55. [57]Puthenveedu MA, von Zastrow M. 2006 Cargo regulates clathrin-coated pit dynamics. Cell 127: 113– 24 17018281
  56. [58]Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL. 2010 Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J. Cell Biol 188: 919– 33 20231386 PMC2845073
  57. [59]Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. 2002 Molecular architecture and functional model of the endocytic AP2 complex. Cell 109: 523– 35 12086608
  58. [60]Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, 2010 Alarge-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141: 1220– 29 20603002 PMC3655264
  59. [61]Kirchhausen T, Owen D, Harrison SC. 2014 Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb. Perspect. Biol 6: a016725 24789820 PMC3996469
  60. [62]Mishra SK, Hawryluk MJ, Brett TJ, Keyel PA, Dupin AL, 2004 Dual engagement regulation of protein interactions with the AP-2 adaptor α appendage. J. Biol. Chem 279: 46191– 203 15292237
  61. [63]Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, 2006 Role of the AP2 β-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLOS. Biol 4: e262 16903783 PMC1540706
  62. [64]Praefcke GJ, Ford MG, Schmid EM, Olesen LE, Gallop JL, 2004 Evolving nature of the AP2 α-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 23: 4371– 83 15496985 PMC526462
  63. [65]Shih W, Gallusser A, Kirchhausen T. 1995 A clathrin-binding site in the hinge of the β2 chain of mammalian AP-2 complexes. J. Biol. Chem 270: 31083– 90 8537368
  64. [66]Owen DJ, Vallis Y, Pearse BMF, McMahon HT, Evans PR. 2000 The structure and function of the ß2-adaptin appendage domain. EMBO J. 19: 4216– 27 10944104 PMC302036
  65. [67]Edeling MA, Mishra SK, Keyel PA, Steinhauser AL, Collins BM, 2006 Molecular switches involving the AP-2 β2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 10: 329– 42 16516836
  66. [69]Hinrichsen L, Harborth J, Andrees L, Weber K, Ungewickell EJ. 2003 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– 70 12960147
  67. [70]Motley AM, Berg N, Taylor MJ, Sahlender DA, Hirst J, 2006 Functional analysis of AP-2 α and μ2 subunits. Mol. Biol. Cell 17: 5298– 308 17035630 PMC1679692
  68. [71]Kelly BT, Graham SC, Liska N, Dannhauser PN, Honing S, 2014 Clathrin adaptors. AP2 controls clathrin polymerization with a membrane-activated switch. Science 345: 459– 63 25061211 PMC4333214
  69. [72]Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, 2010 FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328: 1281– 84 20448150 PMC2883440
  70. [73]Ritter B, Philie J, Girard M, Tung EC, Blondeau F, McPherson PS. 2003 Identification of a family of endocytic proteins that define a new α-adaptin ear-binding motif. EMBO Rep. 4: 1089– 95 14555962 PMC1326374
  71. [74]Umasankar PK, Ma L, Thieman JR, Jha A, Doray B, 2014 A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing. eLife 3: e04137 PMC4215538 25303365
  72. [75]Ma L, Umasankar PK, Wrobel AG, Lymar A, McCoy AJ, 2016 Transient Fcho1/2Eps15/RAP-2 nanoclusters prime the AP-2 clathrin adaptor for cargo binding. Dev. Cell 37: 428– 43 27237791 PMC4921775
  73. [76]Hollopeter G, Lange JJ, Zhang Y, Vu TN, Gu M, 2014 The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. eLife 3: e03648 PMC4215536 25303366
  74. [77]Miller SE, Sahlender DA, Graham SC, Honing S, Robinson MS, 2011 The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147: 1118– 31 22118466 PMC3267021
  75. [79]Ritter B, Murphy S, Dokainish H, Girard M, Gudheti MV, 2013 NECAP 1 regulates AP-2 interactions to control vesicle size, number, and cargo during clathrin-mediated endocytosis. PLOS Biol. 11: e1001670 24130457 PMC3794858
  76. [81]Nunez D, Antonescu C, Mettlen M, Liu A, Schmid SL, 2011 Hotspots organize clathrin-mediated endocytosis by efficient recruitment and retention of nucleating resources. Traffic 12: 1868– 78 21883765 PMC3298691
  77. [82]Smythe E, Ayscough KR. 2003 The Ark1/Prk1 family of protein kinases. Regulators of endocytosis and the actin skeleton. EMBO Rep. 4: 246– 51 12634840 PMC1315904
  78. [83]Ricotta D, Conner SD, Schmid SL, von Figura K, Honing S. 2002 Phosphorylation of the AP2 μ subunit by AAK1 mediates high affinity binding to membrane protein sorting signals. J. Cell Biol 156: 791– 95 11877457 PMC2173304
  79. [84]Olusanya O, Andrews PD, Swedlow JR, Smythe E. 2001 Phosphorylation of threonine 156 of the μ2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo. Curr. Biol 11: 896– 900 11516654
  80. [85]Conner SD, Schroter T, Schmid SL. 2003 AAK1-mediated μ2 phosphorylation is stimulated by assembled clathrin. Traffic 4: 885– 90 14617351
  81. [87]Loerke D, Mettlen M, Schmid SL, Danuser G. 2011 Measuring the hierarchy of molecular events during clathrin-mediated endocytosis. Traffic 12: 815– 25 21447041 PMC3115502
  82. [89]Dannhauser PN, Ungewickell EJ. 2012 Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol 14: 634– 39 22522172
  83. [90]Takei K, Haucke V, Slepnev V, Farsad K, Salazar M, 1998 Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94: 131– 41 9674434
  84. [91]Heuser J 1980 Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol 84: 560– 83 6987244 PMC2110580
  85. [92]Avinoam O, Schorb M, Beese CJ, Briggs JA, Kaksonen M. 2015 Endocytic sites mature by continuous bending and remodeling of the clathrin coat. Science 348: 1369– 72 26089517
  86. [93]Di Paolo G, De Camilli P. 2006 Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651– 57 17035995
  87. [94]Jost M, Simpson F, Kavran JM, Lemmon MA, Schmid SL. 1998 Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol 8: 1399– 402 9889104
  88. [95]Zoncu R, Perera RM, Sebastian R, Nakatsu F, Chen H, 2007 Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. PNAS 104: 3793– 98 17360432 PMC1805489
  89. [96]Antonescu CN, Aguet F, Danuser G, Schmid SL. 2011 Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol. Biol. Cell 22: 2588– 600 21613550 PMC3135483
  90. [97]Perera RM, Zoncu R, Lucast L, De Camilli P, Toomre D. 2006 Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. PNAS 103: 19332– 37 17158794 PMC1693868
  91. [98]Nakatsu F, Perera RM, Lucast L, Zoncu R, Domin J, 2010 The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J. Cell Biol 190: 307– 15 20679431 PMC2922640
  92. [99]Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, 2013 Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499: 233– 37 23823722
  93. [100]Gaidarov I, Smith ME, Domin J, Keen JH. 2001 The class IIphosphoinositide3-kinase C2αis activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell 7: 443– 49 11239472
  94. [101]He K, Marsland R, Upadhyayula S, Song E, Dang S, 2017 Dynamics of phosphoinositide conversion in clathrin-mediated endocytic traffic. Nature 552: 410– 14 29236694 PMC6263037
  95. [102]Daste F, Walrant A, Holst MR, Gadsby JR, Mason J, 2017 Control of actin polymerization via the coincidence of phosphoinositides and high membrane curvature. J. Cell Biol 216: 3745– 65 28923975 PMC5674896
  96. [103]Moore CAC, Milano SK, Benovic JL. 2007 Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol 69: 451– 82 17037978
  97. [104]Cao TT, Mays RW, von Zastrow M. 1998 Regulated endocytosis of G-protein-coupled receptors by a biochemically and functionally distinct subpopulation of clathrin-coated pits. J. Biol. Chem 273: 24592– 602 9733754
  98. [105]Reis CR, Chen PH, Bendris N, Schmid SL. 2017 TRAIL-death receptor endocytosis and apoptosis are selectively regulated by dynamin-1 activation. PNAS 114: 504– 9 28049841 PMC5255607
  99. [106]Smillie KJ, Cousin MA. 2005 Dynamin I phosphorylation and the control of synaptic vesicle endocytosis. Biochem. Soc. Symp 72: 87– 97 PMC2077358 15649133
  100. [107]Schmid SL. 2017 Reciprocal regulation of signaling and endocytosis: implications for the evolving cancer cell. J. Cell Biol 216: 2623– 32 28674108 PMC5584184
  101. [108]Medina M, Wandosell F. 2011 Deconstructing GSK-3: the fine regulation of its activity. Int. J. Alzheimer’s Dis 2011: 479249 21629747 PMC3100567
  102. [109]Reis CR, Chen PH, Srinivasan S, Aguet F, Mettlen M, Schmid SL. 2015 Crosstalk between Akt/GSK3β signaling and dynamin-1 regulates clathrin-mediated endocytosis. EMBO J. 34: 2132– 46 26139537 PMC4557666
  103. [110]Liberali P, Snijder B, Pelkmans L. 2014 A hierarchical map of regulatory genetic interactions in membrane trafficking. Cell 157: 1473– 87 24906158
  104. [111]Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, 2005 Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436: 78– 86 15889048
  105. [112]Schenck A, Goto-Silva L, Collinet C, Rhinn A, Giner A, 2008 The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133: 486– 97 18455989
  106. [113]Pucadyil TJ, Schmid SL. 2009 Conserved functions of membrane active GTPases in coated vesicle formation. Science 325: 1217– 20 19729648 PMC2864031
  107. [114]Chen MS, Obar RA, Schroeder CC, Austin TW, Poodry CA, 1991 Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351: 583– 86 1828536
  108. [115]van der Bliek AM, Meyerowitz EM. 1991 Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351: 411– 14 1674590
  109. [116]Koenig JH, Ikeda K. 1989 Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci 9: 3844– 60 2573698 PMC6569944
  110. [117]Poodiy CA, Hall L, Suzuki DT. 1973 Developmental properties of shibirets1 a pleiotropic mutation affecting larval and adult locomotion and development. Dev. Biol 32: 373– 86 4208027
  111. [118]Damke H, Binns DD, Ueda H, Schmid SL, Baba T. 2001 Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell 12: 2578– 89 11553700 PMC59696
  112. [119]van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL. 1993 Mutations in human dynamin block an intermediate stage in coated vesicle formation. J. Cell Biol 122: 553– 63 8101525 PMC2119674
  113. [120]Damke H, Baba T, Warnock DE, Schmid SL. 1994 Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol 127: 915– 34 7962076 PMC2200053
  114. [121]Warnock DE, Baba T, Schmid SL. 1997 Ubiquitously expressed dynamin-II has a higher intrinsic GTPase activity and a greater propensity for self-assembly than neuronal dynamin-I. Mol. Biol. Cell 8: 2553– 62 9398675 PMC25727
  115. [122]Sochacki KA, Dickey AM, Strub MP, Taraska JW. 2017 Endocytic proteins are partitioned at the edge of the clathrin lattice in mammalian cells. Nat. Cell Biol 19: 352– 61 28346440 PMC7509982
  116. [123]Sever S, Damke H, Schmid SL. 2000 Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J. Cell Biol 150: 1137– 48 10974001 PMC2175254
  117. [124]Sever S, Muhlberg AB, Schmid SL. 1999 Impairment of dynamin’s GAP domain stimulates receptor-mediated endocytosis. Nature 398: 481– 86 10206643
  118. [125]Faelber K, Posor Y, Gao S, Held M, Roske Y, 2011 Crystal structure of nucleotide-free dynamin. Nature 477: 556– 60 21927000
  119. [126]Liu YW, Neumann S, Ramachandran R, Ferguson SM, Pucadyil TJ, Schmid SL. 2011 Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. PNAS 108: E234– 2 21670293 PMC3127893
  120. [127]Neumann S, Schmid SL. 2013 Dual role of BAR domain-containing proteins in regulating vesicle release catalyzed by the GTPase, dynamin-2. J. Biol. Chem 288: 25119– 28 23861397 PMC3757176
  121. [128]Srinivasan S, Dharmarajan V, Reed DK, Griffin PR, Schmid SL. 2016 Identification and function of conformational dynamics in the multidomain GTPase dynamin. EMBO J. 35: 443– 57 26783363 PMC4755114
  122. [129]Zhang X, Shan S-O. 2014 Fidelity of cotranslational protein targeting by the signal recognition particle. Annu. Rev. Biophys 43: 381– 408 24895856 PMC4444370
  123. [130]Kenniston JA, Lemmon MA. 2010 Dynamin GTPase regulation is altered by PH domain mutations found in centronuclear myopathy patients. EMBO J. 29: 3054– 67 20700106 PMC2944063
  124. [131]Krishnan S, Collett M, Robinson PJ. 2015 SH3 domains differentially stimulate distinct dynamin I assembly modes and G domain activity. PLOS ONE 10: e0144609 26659814 PMC4687643
  125. [133]Solomaha E, Palfrey HC. 2005 Conformational changes in dynamin on GTP binding and oligomerization reported by intrinsic and extrinsic fluorescence. Biochem. J 391: 601– 11 15954862 PMC1276961
  126. [134]Shpetner HS, Herskovits JS, Vallee RB. 1996 A binding site for SH3 domains targets dynamin to coated pits. J. Biol. Chem 271: 13– 16 8550547
  127. [135]Cao H, Garcia F, McNiven MA. 1998 Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9: 2595– 609 9725914 PMC25532
  128. [136]Huang Y, Chen-Hwang MC, Dolios G, Murakami N, Padovan JC, 2004 Mnb/Dyrk1A phosphorylation regulates the interaction of dynamin 1 with SH3 domain-containing proteins. Biochemistry 43: 10173– 85 15287745
  129. [137]Xue J, Graham ME, Novelle AE, Sue N, Gray N, 2011 Calcineurin selectively docks with the dynamin Ixb splice variant to regulate activity-dependent bulk endocytosis. J. Biol. Chem 286: 30295– 303 21730063 PMC3162388
  130. [138]Bodmer D, Ascano M, Kuruvilla R. 2011 Isoform-specific dephosphorylation of dynamin1 by calcineurin couples neurotrophin receptor endocytosis to axonal growth. Neuron 70: 1085– 99 21689596 PMC3119854
  131. [139]Chan LS, Hansra G, Robinson PJ, Graham ME. 2010 Differential phosphorylation of dynamin I isoforms in subcellular compartments demonstrates the hidden complexity of phosphoproteomes. J. Proteom. Res 9: 4028– 37 20560669
  132. [140]Di Fiore PP, von Zastrow M. 2014 Endocytosis, signaling, and beyond. Cold Spring Harb. Perspect. Biol 6: a016865 25085911 PMC4107983
  133. [141]Sorkin A, von Zastrow M. 2009 Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol 10: 609– 22 19696798 PMC2895425
  134. [142]Chen PH, Bendris N, Hsiao YJ, Reis CR, Mettlen M, 2017 Crosstalk between CLCb/Dyn1-mediated adaptive clathrin-mediated endocytosis and epidermal growth factor receptor signaling increases metastasis. Dev. Cell 40: 278– 88. 28171750 PMC5740869
  135. [143]Jekely G 2007 Origin of eukaryotic endomembranes: a critical evaluation of different model scenarios. Adv. Exp. Med. Biol 607: 38– 51 17977457
  136. [144]Wideman JG, Leung KF, Field MC, Dacks JB. 2014 The cell biology of the endocytic system from an evolutionary perspective. Cold Spring Harb. Perspect. Biol 6: a016998 24478384 PMC3970418
  137. [145]Rout MP, Field MC. 2017 The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu. Rev. Biochem 86: 637– 57 28471691
  138. [146]Royle SJ. 2006 The cellular functions of clathrin. Cell. Mol. Life Sci 63: 1823– 32 16699812 PMC3475309
  139. [147]Dergai M, Iershov A, Novokhatska O, Pankivskyi S, Rynditch A. 2016 Evolutionary changes on the way to clathrin-mediated endocytosis in animals. Genome Biol. Evol 8: 588– 606 26872775 PMC4824007
  140. [148]Ben-Shlomo I, Yu Hsu S, Rauch R, Kowalski HW, Hsueh AJW. 2003 Signaling receptome: a genomic and evolutionary perspective of plasma membrane receptors involved in signal transduction. Sci. Signal Transduct. Knowl. Environ 187: RE9 12815191
  141. [149]Liu Y-W, Su AI, Schmid SL. 2012 The evolution of dynamin to regulate clathrin-mediated endocytosis: speculations on the evolutionarily late appearance of dynamin relative to clathrin-mediated endocytosis. Bioessays 34: 643– 47 22592980 PMC5715466
  142. [150]Elde NC, Morgan G, Winey M, Sperling L, Turkewitz AP. 2005 Elucidation of clathrin-mediated endocytosis in tetrahymena reveals an evolutionarily convergent recruitment of dynamin. PLOS Genet. 1: e52 16276403 PMC1277907
  143. [151]Huang KM, D’Hondt K, Riezman H, Lemmon SK. 1999 Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J. 18: 3897– 908 10406795 PMC1171466
  144. [152]Reubold TF, Faelber K, Plattner N, Posor Y, Ketel K, 2015 Crystal structure of the dynamin tetramer. Nature 525: 404– 8 26302298

Cited by

Sorted by citations

Authors
Mettlen, M., Chen, P.-H., Srinivasan, S., Danuser, G., & Schmid, S. L.
Affiliations
The University of Texas Southwestern Medical Center (US)
ORCID
Venue
Annual Review of Biochemistry
Publisher
Annual Reviews
Published
2018-06-20
Volume
87
Issue
1
Pages
871-896
ISSN
  • 0066-4154 (ISSN-L)
  • 1545-4509
DOI
10.1146/annurev-biochem-062917-012644
PMC
PMC6383209
OpenAlex
W2800413193
Cited by
614
References
7
Citations by year
2026: 58 · 2025: 92 · 2024: 92 · 2023: 80 · 2022: 85 · 2021: 86 · 2020: 73 · 2019: 38 · 2018: 10
FWCI
5.82
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Biochemistry (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Science Council (103-2917-I-564-029)
  • National Institutes of Health (MH61345)
  • National Institute of Mental Health (R01MH061345, MH61345, R37MH061345)
  • National Institute of General Medical Sciences (R01GM073165, GM-42455, R01GM042455, GM73165)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords
clathrin-mediated endocytosis, clathrin-coated pits, clathrin-coated vesicles, adaptor protein complexes, dynamin, post-translational modification, allosteric conformational change, splice variants, cargo selection, membrane remodeling, cell surface signaling
MeSH terms
Allosteric Regulation, Animals, Clathrin, Endocytosis, Humans, Models, Biological, Phosphorylation, Protein Conformation, Signal Transduction, Phosphatidylinositol Phosphates, Evolution, Molecular, Clathrin-Coated Vesicles, Adaptor Protein Complex 2, Dynamins

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