Endocytic pathways and endosomal trafficking: a primer

Roth TF, Porter KR. Yolk Protein Uptake in the Oocyte of the Mosquito Aedes Aegypti. L. J Cell Biol. 1964;20:313–32.

Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol. 1955;1(5):445–58.

Moya M, et al. Inhibition of coated pit formation in Hep2 cells blocks the cytotoxicity of diphtheria toxin but not that of ricin toxin. J Cell Biol. 1985;101(2):548–59.

Hansen SH, Sandvig K, van Deurs B. The preendosomal compartment comprises distinct coated and noncoated endocytic vesicle populations. J Cell Biol. 1991;113(4):731–41.

Lamaze C, et al. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell. 2001;7(3):661–71.

Kirkham M, et al. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol. 2005;168(3):465–76.

Scott CC, Vacca F, Gruenberg J. Endosome maturation, transport and functions. Semin Cell Dev Biol. 2014;31:2–10.

Preston JE, Abbott NJ, Begley DJ. Transcytosis of macromolecules at the blood-brain barrier. Adv Pharmacol. 2014;71:147–63.

Antonescu CN, McGraw TE, Klip A. Reciprocal regulation of endocytosis and metabolism. Cold Spring Harb Perspect Biol. 2014;6(7):a016964.

Irannejad R, von Zastrow M. GPCR signaling along the endocytic pathway. Curr Opin Cell Biol. 2014;27:109–16.

Goh LK, Sorkin A. Endocytosis of receptor tyrosine kinases. Cold Spring Harb Perspect Biol. 2013;5(5):a017459.

Mellman I, Yarden Y. Endocytosis and cancer. Cold Spring Harb Perspect Biol. 2013;5(12):a016949.

Carpentier JL, et al. Co-localization of 125I-epidermal growth factor and ferritin-low density lipoprotein in coated pits: a quantitative electron microscopic study in normal and mutant human fibroblasts. J Cell Biol. 1982;95(1):73–7.

Neutra MR, et al. Intracellular transport of transferrin- and asialoorosomucoid-colloidal gold conjugates to lysosomes after receptor-mediated endocytosis. J Histochem Cytochem. 1985;33(11):1134–44.

Robinson MS. Forty Years of Clathrin-coated Vesicles. Traffic. 2015;16(12)1210–38.

Kirchhausen T, Owen D, Harrison SC. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb Perspect Biol. 2014;6(5):a016725.

Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol. 1999;15:705–32.

McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–33.

Traub LM, Bonifacino JS. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol. 2013;5(11):a016790.

Cocucci E, et al. The first five seconds in the life of a clathrin-coated pit. Cell. 2012;150(3):495–507.

Henne WM, et al. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science. 2010;328(5983):1281–4.

Woodward MP, Roth TF. Coated vesicles: characterization, selective dissociation, and reassembly. Proc Natl Acad Sci U S A. 1978;75(9):4394–8.

Qualmann B, Koch D, Kessels MM. Let’s go bananas: revisiting the endocytic BAR code. EMBO J. 2011;30(17):3501–15.

Aguet F, et al. Advances in analysis of low signal-to-noise images link dynamin and AP2 to the functions of an endocytic checkpoint. Dev Cell. 2013;26(3):279–91.

Schmid SL, Frolov VA. Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol. 2011;27:79–105.

Ferguson SM, et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell. 2009;17(6):811–22.

Rothman JE, Schmid SL. Enzymatic recycling of clathrin from coated vesicles. Cell. 1986;46(1):5–9.

Ungewickell E, et al. Role of auxilin in uncoating clathrin-coated vesicles. Nature. 1995;378(6557):632–5.

Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007;8(3):185–94.

Pelkmans L, Helenius A. Endocytosis via caveolae. Traffic. 2002;3(5):311–20.

Murata M, et al. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A. 1995;92(22):10339–43.

Harder T, Simons K. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr Opin Cell Biol. 1997;9(4):534–42.

Parton RG, del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol. 2013;14(2):98–112.

Nassar ZD, Parat MO. Cavin family: new players in the biology of caveolae. Int Rev Cell Mol Biol. 2015;320:235–305.

Kiss AL. Caveolae and the regulation of endocytosis. Adv Exp Med Biol. 2012;729:14–28.

Li S, Seitz R, Lisanti MP. Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem. 1996;271(7):3863–8.

Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol. 1994;127(5):1199–215.

Henley JR, et al. Dynamin-mediated internalization of caveolae. J Cell Biol. 1998;141(1):85–99.

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. 1990;265(11):6382–8.

Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem. 2009;78:857–902.

Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol. 2011;12(6):362–75.

Mayor S, Parton RG, Donaldson JG. Clathrin-independent pathways of endocytosis. In: Schmid ASSL, Zerial M, editor. Endocytosis. 2016. p. pii:a016758. (Cold Spring Harb Perspect Biol).

Boucrot E, et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 2015;517(7535):460–5.

Huotari J, Helenius A. Endosome maturation. EMBO J. 2011;30(17):3481–500.

Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol. 1997;139(1):49–61.

Glebov OO, Bright NA, Nichols BJ. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol. 2006;8(1):46–54.

Frick M, et al. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol. 2007;17(13):1151–6.

Mayor S, Parton RG, Donaldson JG. Clathrin-independent pathways of endocytosis. Cold Spring Harb Perspect Biol. 2014;6:6.

Maldonado-Baez L, Williamson C, Donaldson JG. Clathrin-independent endocytosis: a cargo-centric view. Exp Cell Res. 2013;319(18):2759–69.

Bitsikas V, Correa IR Jr, Nichols BJ. Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife. 2014;3:e03970.

Elkin SR, et al. A systematic analysis reveals heterogeneous changes in the endocytic activities of cancer cells. Cancer Res. 2015;75(21):4640–50.

Salzman NH, Maxfield FR. Intracellular fusion of sequentially formed endocytic compartments. J Cell Biol. 1988;106(4):1083–91.

Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem. 1986;55:663–700.

Fuchs R, Schmid SL, Mellman I. A possible role for the Na+, K+-ATPase in regulating ATP-dependent endosome acidification. Proc. Natl. Acad. Sci. (USA). 1989;86(2):539–43

Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443(7112):651–7.

Bissig C, Gruenberg J. Lipid sorting and multivesicular endosome biogenesis. Cold Spring Harb Perspect Biol. 2013;5(10):a016816.

Lemmon MA. Phosphoinositide recognition domains. Traffic. 2003;4(4):201–13.

Balla T. Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci. 2005;118(Pt 10):2093–104.

Gillooly DJ, et al. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 2000;19(17):4577–88.

Klumperman J, Raposo G. The complex ultrastructure of the endolysosomal system. Cold Spring Harb Perspect Biol. 2014;6(10):a016857.

Schu PV, et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 1993;260(5104):88–91.

Odorizzi G, Babst M, Emr SD. Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci. 2000;25(5):229–35.

Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2(2):107–17.

Shin HW, et al. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol. 2005;170(4):607–18.

Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol. 1997;9(4):496–504.

Mellman I. Endocytosis and molecular sorting. Annu Rev Cell Dev Biol. 1996;12:575–625.

Maxfield FR, McGraw TE. Endocytic recycling. Nat Rev Mol Cell Biol. 2004;5(2):121–32.

Hsu VW, Bai M, Li J. Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol. 2012;13(5):323–8.

van Weering JR, et al. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J. 2012;31(23):4466–80.

Burd C, Cullen PJ. Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol. 2014;6:2.

Seaman MN, et al. Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J Cell Biol. 1997;137(1):79–92.

Seaman MN, McCaffery JM, Emr SD. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol. 1998;142(3):665–81.

Babst M. MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol. 2011;23(4):452–7.

Hurley JH, Hanson PI. Membrane budding and scission by the ESCRT machinery: it’s all in the neck. Nat Rev Mol Cell Biol. 2010;11(8):556–66.

Henne WM, Stenmark H, Emr SD. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol. 2013;5:9.

Mitsunari T, et al. Clathrin adaptor AP-2 is essential for early embryonal development. Mol Cell Biol. 2005;25(21):9318–23.

Royle SJ. The cellular functions of clathrin. Cell Mol Life Sci. 2006;63(16):1823–32.

Song Y, et al. Caveolin-1 knockdown is associated with the metastasis and proliferation of human lung cancer cell line NCI-H460. Biomed Pharmacother. 2012;66(6):439–47.

Zhan P, et al. Expression of caveolin-1 is correlated with disease stage and survival in lung adenocarcinomas. Oncol Rep. 2012;27(4):1072–8.

Sunaga N, et al. Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res. 2004;64(12):4277–85.

Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol. 2005;6(2):112–26.

Howes MT, et al. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. J Cell Biol. 2010;190(4):675–91.

Cossart P, Helenius A. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol. 2014;6:8.

Adjei IM, Sharma B, Labhasetwar V. Nanoparticles: cellular uptake and cytotoxicity. Adv Exp Med Biol. 2014;811:73–91.

Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009;10(8):513–25.

Seabra MC, Mules EH, Hume AN. Rab GTPases, intracellular traffic and disease. Trends Mol Med. 2002;8(1):23–30.

Cheng KW, et al. Emerging role of RAB GTPases in cancer and human disease. Cancer Res. 2005;65(7):2516–9.

Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91(1):119–49.

Sharma S, Skowronek A, Erdmann KS. The role of the Lowe syndrome protein OCRL in the endocytic pathway. Biol Chem. 2015;396(12):1293–300.

Esposito G, Clara AF, Verstreken P. Synaptic vesicle trafficking and Parkinson’s disease. Dev Neurobiol. 2012;72(1):134–44.

Jiang S, et al. Trafficking regulation of proteins in Alzheimer’s disease. Mol Neurodegener. 2014;9:6.

Goldenring JR. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat Rev Cancer. 2013;13(11):813–20.

Gauthier NC, Masters TA, Sheetz MP. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 2012;22(10):527–35.

Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6(11):a022616.

Pfeffer SR. Rab GTPase regulation of membrane identity. Curr Opin Cell Biol. 2013;25(4):414–9.

Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol. 2010;22(4):461–70.

Gurkan C, et al. Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol Biol Cell. 2005;16(8):3847–64.