Clathrin-independent endocytosis: A cargo-centric view

Experimental Cell Research

Volumn 319, Issue 18, 2013, Pages 2759-2769

  Maldonado Báez, Lymarie ^a   Williamson, Chad ^a   Donaldson, Julie G ^a  

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

Author keywords

Cell adhesion molecules; Clathrin independent endocytosis; Endocytosis; Ion channels; Nutrient transporters; Plasma membrane protein; Protein sorting

Indexed keywords

AMINO ACID; BACTERIAL TOXIN; CD147 ANTIGEN; CD98 ANTIGEN; CELL ADHESION MOLECULE; CLATHRIN; G PROTEIN COUPLED RECEPTOR; GLUCOSE TRANSPORTER 1; GROWTH FACTOR; HERMES ANTIGEN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; ION CHANNEL; LAT1 PROTEIN; SYNDECAN; UNCLASSIFIED DRUG; UVOMORULIN;

AUTOIMMUNITY; CELL ADHESION; CELL FATE; CELL SELECTION; CELL SURFACE; ENDOCYTOSIS; ENDOSOME; HUMAN; IMMUNE SYSTEM; INTERNALIZATION; ION TRANSPORT; MOLECULAR RECOGNITION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

BACTERIA (MICROORGANISMS);

EID: 84886235335     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.08.008     Document Type: Review

References (115)

1. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
2. Traub L.M. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell. Biol. 2009, 10:583-596.
3. Sandvig K., Torgersen M.L., Raa H.A., van Deurs B. Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem. Cell. Biol. 2008, 129:267-276.
4. Howes M.T., Kirkham M., Riches J., Cortese K., Walser P.J., Simpson F., Hill M.M., Jones A., Lundmark R., Lindsay M.R., Hernandez-Deviez D.J., Hadzic G., McCluskey A., Bashir R., Liu L., Pilch P., McMahon H., Robinson P.J., Hancock J.F., Mayor S., Parton R.G. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J. Cell. Biol. 2010, 190:675-691.
5. Kumari S., Mayor S. ARF1 is directly involved in dynamin-independent endocytosis. Nat. Cell. Biol. 2008, 10:30-41.
6. 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 2002, 2:411-423.
7. Brown F.D., Rozelle A.L., Yin H.L., Balla T., Donaldson J.G. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 2001, 154:1007-1017.
8. 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 2003, 14:417-431.
9. Radhakrishna H., Donaldson J.G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 1997, 139:49-61.
10. Lamaze C., Dujeancourt A., Baba T., Lo C.G., Benmerah A., Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 2001, 7:661-671.
11. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat. Cell Biol. 2006, 8:46-54.
12. Parton R.G., del Pozo M.A. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev. Mol. Cell Biol. 2013, 14:98-112.
13. Donaldson J.G., Porat-Shliom N., Cohen L.A. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal. 2009, 21:1-6.
14. Naslavsky N., Weigert R., Donaldson J.G. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 2004, 15:3542-3552.
15. Grant B.D., Donaldson J.G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 2009, 10:597-608.
16. Powelka A.M., Sun J., Li J., Gao M., Shaw L.M., Sonnenberg A., Hsu V.W. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 2004, 5:20-36.
17. Aikawa Y., Martin T.F. ADP-ribosylation factor 6 regulation of phosphatidylinositol-4,5-bisphosphate synthesis, endocytosis, and exocytosis. Methods Enzymol. 2005, 404:422-431.
18. Balklava Z., Pant S., Fares H., Grant B.D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 2007, 9:1066-1073.
19. Naslavsky N., Rahajeng J., Sharma M., Jovic M., Caplan S. Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol. Biol. Cell 2006, 17:163-177.
20. Robertson S.E., Setty S.R., Sitaram A., Marks M.S., Lewis R.E., Chou M.M. Extracellular signal-regulated kinase regulates clathrin-independent endosomal trafficking. Mol. Biol. Cell 2006, 17:645-657.
21. Shi A., Pant S., Balklava Z., Chen C.C., Figueroa V., Grant B.D. A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport. Curr. Biol. 2007, 17:1913-1924.
22. Walseng E., Bakke O., Roche P.A. MHC class II-peptide complexes internalize using a clathrin- and dynamin-independent endocytosis pathway. J. Biol. Chem. 2008, 283:14717-14727.
23. Weigert R., Yeung A.C., Li J., Donaldson J.G. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol. Biol. Cell 2004, 15:3758-3770.
24. Eyster C.A., Higginson J.D., Huebner R., Porat-Shliom N., Weigert R., Wu W.W., Shen R.F., Donaldson J.G. Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 2009, 10:590-599.
25. Eyster C.A., Cole N.B., Petersen S., Viswanathan K., Fruh K., Donaldson J.G. MARCH ubiquitin ligases alter the itinerary of clathrin-independent cargo from recycling to degradation. Mol. Biol. Cell 2011, 22:3218-3230.
26. Barral D.C., Cavallari M., McCormick P.J., Garg S., Magee A.I., Bonifacino J.S., De Libero G., Brenner M.B. CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 2008, 9:1446-1457.
27. Barral D.C., Garg S., Casalou C., Watts G.F., Sandoval J.L., Ramalho J.S., Hsu V.W., Brenner M.B. Arl13b regulates endocytic recycling traffic. Proc. Natl. Acad. Sci. USA 2012, 109:21354-21359.
28. Odorizzi C.G., Trowbridge I.S., Xue L., Hopkins C.R., Davis C.D., Collawn J.F. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment. J. Cell Biol. 1994, 126:317-330.
29. Dugast M., Toussaint H., Dousset C., Benaroch P. AP2 clathrin adaptor complex, but not AP1, controls the access of the major histocompatibility complex (MHC) class II to endosomes. J. Biol. Chem. 2005, 280:19656-19664.
30. Risitano A.M. Paroxysmal nocturnal hemoglobinuria and other complement-mediated hematological disorders. Immunobiology 2012, 217:1080-1087.
31. Kimberley F.C., Sivasankar B., Paul Morgan B. Alternative roles for CD59. Mol. Immunol. 2007, 44:73-81.
32. Patel K.P., Coyne C.B., Bergelson J.M. Dynamin- and lipid raft-dependent entry of decay-accelerating factor (DAF)-binding and non-DAF-binding coxsackieviruses into nonpolarized cells. J. Virol. 2009, 83:11064-11077.
33. Riento K., Frick M., Schafer I., Nichols B.J. Endocytosis of flotillin-1 and flotillin-2 is regulated by Fyn kinase. J. Cell Sci. 2009, 122:912-918.
34. Antony A.C. The biological chemistry of folate receptors. Blood 1992, 79:2807-2820.
35. Karacsonyi C., Miguel A.S., Puertollano R. Mucolipin-2 localizes to the Arf6-associated pathway and regulates recycling of GPI-APs. Traffic 2007, 8:1404-1414.
36. Yang Y., Liang B., Liu J., Li J., Grunnet M., Olesen S.P., Rasmussen H.B., Ellinor P.T., Gao L., Lin X., Li L., Wang L., Xiao J., Liu Y., Zhang S., Liang D., Peng L., Jespersen T., Chen Y.H. Identification of a Kir3.4 mutation in congenital long QT syndrome. Am. J. Hum. Genet. 2010, 86:872-880.
37. Gong Q., Weide M., Huntsman C., Xu Z., Jan L.Y., Ma D. Identification and characterization of a new class of trafficking motifs for controlling clathrin-independent internalization and recycling. J. Biol. Chem. 2007, 282:13087-13097.
38. Ganapathy V., Thangaraju M., Prasad P.D. Nutrient transporters in cancer: relevance to Warburg hypothesis and beyond. Pharmacol. Ther. 2009, 121:29-40.
39. Augustin R. The protein family of glucose transport facilitators: it is not only about glucose after all. IUBMB Life 2010, 62:315-333.
40. Brockmann K. The expanding phenotype of GLUT1-deficiency syndrome. Brain Dev. 2009, 31:545-552.
41. Kanai Y., Segawa H., Miyamoto K., Uchino H., Takeda E., Endou H. Expression cloning and characterization of a transporter for large neutral amino acids activated by the heavy chain of 4F2 antigen (CD98). J. Biol. Chem. 1998, 273:23629-23632.
42. Mastroberardino L., Spindler B., Pfeiffer R., Skelly P.J., Loffing J., Shoemaker C.B., Verrey F. Amino-acid transport by heterodimers of 4F2hc/CD98 and members of a permease family. Nature 1998, 395:288-291.
43. Rautio J., Gynther M., Laine K. LAT1-mediated prodrug uptake: a way to breach the blood-brain barrier?. Ther. Deliv. 2013, 4:281-284.
44. Sinclair L.V., Rolf J., Emslie E., Shi Y.B., Taylor P.M., Cantrell D.A. Control of amino-acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation. Nat. Immunol. 2013, 14:500-508.
45. Twigg M.W., Freestone K., Homer-Vanniasinkam S., Ponnambalam S. The LOX-1 scavenger receptor and its implications in the treatment of vascular disease. Cardiol. Res. Pract. 2012, 2012:632408.
46. Yoshimoto R., Fujita Y., Kakino A., Iwamoto S., Takaya T., Sawamura T. The discovery of LOX-1, its ligands and clinical significance. Cardiovasc. Drugs Ther. 2011, 25:379-391.
47. Murphy J.E., Vohra R.S., Dunn S., Holloway Z.G., Monaco A.P., Homer-Vanniasinkam S., Walker J.H., Ponnambalam S. Oxidised LDL internalisation by the LOX-1 scavenger receptor is dependent on a novel cytoplasmic motif and is regulated by dynamin-2. J. Cell Sci. 2008, 121:2136-2147.
48. Scotti E., Calamai M., Goulbourne C.N., Zhang L., Hong C., Lin R.R., Choi J., Pilch P.F., Fong L.G., Zou P., Ting A.Y., Pavone F.S., Young S.G., Tontonoz P. IDOL stimulates clathrin-independent endocytosis and multivesicular body-mediated lysosomal degradation of the low-density lipoprotein receptor. Mol. Cell Biol. 2013, 33:1503-1514.
49. Lavezzari G., Roche K.W. Constitutive endocytosis of the metabotropic glutamate receptor mGluR7 is clathrin-independent. Neuropharmacology 2007, 52:100-107.
50. Scarselli M., Donaldson J.G. Constitutive internalization of G protein-coupled receptors and G proteins via clathrin-independent endocytosis. J. Biol. Chem. 2009, 284:3577-3585.
51. Sigismund S., Argenzio E., Tosoni D., Cavallaro E., Polo S., Di Fiore P.P. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell. 2008, 15:209-219.
52. Parachoniak C.A., Luo Y., Abella J.V., Keen J.H., Park M. GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev. Cell 2011, 20:751-763.
53. Long E.O. ICAM-1: getting a grip on leukocyte adhesion. J. Immunol. 2011, 186:5021-5023.
54. Marlin S.D., Springer T.A. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell 1987, 51:813-819.
55. Smith C.W., Marlin S.D., Rothlein R., Toman C., Anderson D.C. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J. Clin. Invest. 1989, 83:2008-2017.
56. Muro S., Wiewrodt R., Thomas A., Koniaris L., Albelda S.M., Muzykantov V.R., Koval M. A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J. Cell Sci. 2003, 116:1599-1609.
57. Greve J.M., Davis G., Meyer A.M., Forte C.P., Yost S.C., Marlor C.W., Kamarck M.E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell 1989, 56:839-847.
58. Staunton D.E., Merluzzi V.J., Rothlein R., Barton R., Marlin S.D., Springer T.A. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 1989, 56:849-853.
59. Selinka H.C., Zibert A., Wimmer E. Poliovirus can enter and infect mammalian cells by way of an intercellular adhesion molecule 1 pathway. Proc. Natl. Acad. Sci. USA 1991, 88:3598-3602.
60. Paterson A.D., Parton R.G., Ferguson C., Stow J.L., Yap A.S. Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J. Biol. Chem. 2003, 278:21050-21057.
61. Kourtidis A., Ngok S.P., Anastasiadis P.Z. p120 Catenin: an essential regulator of cadherin stability, adhesion-induced signaling, and cancer progression. Prog. Mol. Biol. Transl. Sci. 2013, 116:409-432.
62. Alexopoulou A.N., Multhaupt H.A., Couchman J.R. Syndecans in wound healing, inflammation and vascular biology. Int. J. Biochem. Cell Biol. 2007, 39:505-528.
63. Wilsie L.C., Gonzales A.M., Orlando R.A. Syndecan-1 mediates internalization of apoE-VLDL through a low density lipoprotein receptor-related protein (LRP)-independent, non-clathrin-mediated pathway. Lipids Health Dis. 2006, 5:23.
64. Fuki I.V., Meyer M.E., Williams K.J. Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 2000, 351(Pt 3):607-612.
65. Zimmermann P., Zhang Z., Degeest G., Mortier E., Leenaerts I., Coomans C., Schulz J., N'Kuli F., Courtoy P.J., David G. Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 2005, 9:377-388.
66. Morgan M.R., Hamidi H., Bass M.D., Warwood S., Ballestrem C., Humphries M.J. Syndecan-4 phosphorylation is a control point for integrin recycling. Dev. Cell 2013, 24:472-485.
67. Bobardt M.D., Chatterji U., Schaffer L., de Witte L., Gallay P.A. Syndecan-Fc hybrid molecule as a potent in vitro microbicidal anti-HIV-1 agent. Antimicrob. Agents Chemother. 2010, 54:2753-2766.
68. Shi Q., Jiang J., Luo G. Syndecan-1 serves as the major receptor for attachment of hepatitis C virus to the surfaces of hepatocytes. J. Virol. 2013, 87:6866-6875.
69. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
70. Feire A.L., Koss H., Compton T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. USA 2004, 101:15470-15475.
71. Aruffo A., Stamenkovic I., Melnick M., Underhill C.B., Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990, 61:1303-1313.
72. Ponta H., Sherman L., Herrlich P.A. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 2003, 4:33-45.
73. Toole B.P. Hyaluronan-CD44 interactions in cancer: paradoxes and possibilities. Clin. Cancer Res. 2009, 15:7462-7468.
74. Schrager H.M., Alberti S., Cywes C., Dougherty G.J., Wessels M.R. Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of group A Streptococcus to CD44 on human keratinocytes. J. Clin. Invest. 1998, 101:1708-1716.
75. Mackay C.R., Terpe H.J., Stauder R., Marston W.L., Stark H., Gunthert U. Expression and modulation of CD44 variant isoforms in humans. J. Cell Biol. 1994, 124:71-82.
76. Jones M., Tussey L., Athanasou N., Jackson D.G. Heparan sulfate proteoglycan isoforms of the CD44 hyaluronan receptor induced in human inflammatory macrophages can function as paracrine regulators of fibroblast growth factor action. J. Biol. Chem. 2000, 275:7964-7974.
77. Saksela O., Moscatelli D., Sommer A., Rifkin D.B. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol. 1988, 107:743-751.
78. Tsukita S., Oishi K., Sato N., Sagara J., Kawai A. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 1994, 126:391-401.
79. Thankamony S.P., Knudson W. Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J. Biol. Chem. 2006, 281:34601-34609.
80. Cantor J.M., Ginsberg M.H. CD98 at the crossroads of adaptive immunity and cancer. J. Cell Sci. 2012, 125:1373-1382.
81. Nguyen H.T., Merlin D. Homeostatic and innate immune responses: role of the transmembrane glycoprotein CD98. Cell Mol. Life Sci. 2012, 69:3015-3026.
82. Liu X., Charrier L., Gewirtz A., Sitaraman S., Merlin D. CD98 and intracellular adhesion molecule I regulate the activity of amino acid transporter LAT-2 in polarized intestinal epithelia. J. Biol. Chem. 2003, 278:23672-23677.
83. Zent R., Fenczik C.A., Calderwood D.A., Liu S., Dellos M., Ginsberg M.H. Class- and splice variant-specific association of CD98 with integrin beta cytoplasmic domains. J. Biol. Chem. 2000, 275:5059-5064.
84. Feral C.C., Zijlstra A., Tkachenko E., Prager G., Gardel M.L., Slepak M., Ginsberg M.H. CD98hc (SLC3A2) participates in fibronectin matrix assembly by mediating integrin signaling. J. Cell Biol. 2007, 178:701-711.
85. Lemaitre G., Stella A., Feteira J., Baldeschi C., Vaigot P., Martin M.T., Monsarrat B., Waksman G. CD98hc (SLC3A2) is a key regulator of keratinocyte adhesion. J. Dermatol. Sci. 2011, 61:169-179.
86. Chandrasekaran S., Guo N.H., Rodrigues R.G., Kaiser J., Roberts D.D. Pro-adhesive and chemotactic activities of thrombospondin-1 for breast carcinoma cells are mediated by alpha3beta1 integrin and regulated by insulin-like growth factor-1 and CD98. J. Biol. Chem. 1999, 274:11408-11416.
87. Yan Y., Vasudevan S., Nguyen H.T., Merlin D. Intestinal epithelial CD98: an oligomeric and multifunctional protein. Biochim. Biophys. Acta 2008, 1780:1087-1092.
88. Parmacek M.S., Karpinski B.A., Gottesdiener K.M., Thompson C.B., Leiden J.M. Structure, expression and regulation of the murine 4F2 heavy chain. Nucleic Acids Res. 1989, 17:1915-1931.
89. Bellone G., Alloatti G., Levi R., Geuna M., Tetta C., Peruzzi L., Letarte M., Malavasi F. Identification of a new epitope of the 4F2/44D7 molecular complex present on sarcolemma and isolated cardiac fibers. Eur. J. Immunol. 1989, 19:1-8.
90. Dixon W.T., Sikora L.K., Demetrick D.J., Jerry L.M. Isolation and characterization of a heterodimeric surface antigen on human melanoma cells and evidence that it is the 4F2 cell activation/proliferation molecule. Int. J. Cancer 1990, 45:59-68.
91. Dalton P., Christian H.C., Redman C.W., Sargent I.L., Boyd C.A. Membrane trafficking of CD98 and its ligand galectin 3 in BeWo cells-implication for placental cell fusion. FEBS J. 2007, 274:2715-2727.
92. Schroeder N., Chung C.S., Chen C.H., Liao C.L., Chang W. The lipid raft-associated protein CD98 is required for vaccinia virus endocytosis. J. Virol. 2012, 86:4868-4882.
93. Huet E., Gabison E.E., Mourah S., Menashi S. Role of emmprin/CD147 in tissue remodeling. Connect. Tissue Res. 2008, 49:175-179.
94. Tang W., Hemler M.E. Caveolin-1 regulates matrix metalloproteinases-1 induction and CD147/EMMPRIN cell surface clustering. J. Biol. Chem. 2004, 279:11112-11118.
95. Berditchevski F., Chang S., Bodorova J., Hemler M.E. Generation of monoclonal antibodies to integrin-associated proteins. Evidence that alpha3beta1 complexes with EMMPRIN/basigin/OX47/M6. J. Biol. Chem. 1997, 272:29174-29180.
96. Schreiner A., Ruonala M., Jakob V., Suthaus J., Boles E., Wouters F., Starzinski-Powitz A. Junction protein shrew-1 influences cell invasion and interacts with invasion-promoting protein CD147. Mol. Biol. Cell 2007, 18:1272-1281.
97. Kirk P., Wilson M.C., Heddle C., Brown M.H., Barclay A.N., Halestrap A.P. CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J. 2000, 19:3896-3904.
98. Pushkarsky T., Zybarth G., Dubrovsky L., Yurchenko V., Tang H., Guo H., Toole B., Sherry B., Bukrinsky M. CD147 facilitates HIV-1 infection by interacting with virus-associated cyclophilin A. Proc. Natl. Acad. Sci. USA 2001, 98:6360-6365.
99. Crosnier C., Bustamante L.Y., Bartholdson S.J., Bei A.K., Theron M., Uchikawa M., Mboup S., Ndir O., Kwiatkowski D.P., Duraisingh M.T., Rayner J.C., Wright G.J. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 2011, 480:534-537.
100. Bonifacino J.S., Lippincott-Schwartz J. Coat proteins: shaping membrane transport. Nat. Rev. Mol. Cell Biol. 2003, 4:409-414.
101. Maldonado-Baez L., Cole N.B., Kramer H., Donaldson J.G. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell Biol. 2013, 201:233-247.
102. Thorne R.F., Legg J.W., Isacke C.M. The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J. Cell Sci. 2004, 117:373-380.
103. Walenta J.H., Didier A.J., Liu X., Kramer H. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 2001, 152:923-934.
104. Cai B., Caplan S., Naslavsky N. cPLA2alpha and EHD1 interact and regulate the vesiculation of cholesterol-rich, GPI-anchored, protein-containing endosomes. Mol. Biol. Cell 2012, 23:1874-1888.
105. Cai B., Katafiasz D., Horejsi V., Naslavsky N. Pre-sorting endosomal transport of the GPI-anchored protein, CD59, is regulated by EHD1. Traffic 2011, 12:102-120.
106. Brandstaetter H., Kendrick-Jones J., Buss F. Myo1c regulates lipid raft recycling to control cell spreading, migration and Salmonella invasion. J. Cell Sci. 2012, 125:1991-2003.
107. Piper R.C., Katzmann D.J. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 2007, 23:519-547.
108. Raiborg C., Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458:445-452.
109. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70:503-533.
110. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.
111. Allaire P.D., Marat A.L., Dall'Armi C., Di Paolo G., McPherson P.S., Ritter B. The Connecdenn DENN domain: a GEF for Rab35 mediating cargo-specific exit from early endosomes. Mol. Cell 2010, 37:370-382.
112. Miaczynska M., Christoforidis S., Giner A., Shevchenko A., Uttenweiler-Joseph S., Habermann B., Wilm M., Parton R.G., Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004, 116:445-456.
113. Chen P.I., Kong C., Su X., Stahl P.D. Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J. Biol. Chem. 2009, 284:30328-30338.
114. Steinberg F., Gallon M., Winfield M., Thomas E.C., Bell A.J., Heesom K.J., Tavare J.M., Cullen P.J. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 2013, 15:461-471.
115. Masedunskas A., Weigert R. Intravital two-photon microscopy for studying the uptake and trafficking of fluorescently conjugated molecules in live rodents. Traffic 2008, 9:1801-1810.