Skip to main content
Erschienen in: Wiener Medizinische Wochenschrift 7-8/2016

01.05.2016 | main topic

Endocytic pathways and endosomal trafficking: a primer

verfasst von: Sarah R. Elkin, Ashley M. Lakoduk, Sandra L. Schmid, PhD

Erschienen in: Wiener Medizinische Wochenschrift | Ausgabe 7-8/2016

Einloggen, um Zugang zu erhalten

Summary

This brief overview of endocytic trafficking is written in honor of Renate Fuchs, who retires this year. In the mid-1980s, Renate pioneered studies on the ion-conducting properties of the recently discovered early and late endosomes and the mechanisms governing endosomal acidification. As described in this review, after uptake through one of many mechanistically distinct endocytic pathways, internalized proteins merge into a common early/sorting endosome. From there they again diverge along distinct sorting pathways, back to the cell surface, on to the trans-Golgi network or across polarized cells. Other transmembrane receptors are packaged into intraluminal vesicles of late endosomes/multivesicular bodies that eventually fuse with and deliver their content to lysosomes for degradation. Endosomal acidification, in part, determines sorting along this pathway. We describe other sorting machinery and mechanisms, as well as the rab proteins and phosphatidylinositol lipids that serve to dynamically define membrane compartments along the endocytic pathway.
Literatur
3.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
4.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
5.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
6.
7.
Zurück zum Zitat Scott CC, Vacca F, Gruenberg J. Endosome maturation, transport and functions. Semin Cell Dev Biol. 2014;31:2–10.CrossRefPubMed Scott CC, Vacca F, Gruenberg J. Endosome maturation, transport and functions. Semin Cell Dev Biol. 2014;31:2–10.CrossRefPubMed
8.
Zurück zum Zitat Preston JE, Abbott NJ, Begley DJ. Transcytosis of macromolecules at the blood-brain barrier. Adv Pharmacol. 2014;71:147–63.CrossRefPubMed Preston JE, Abbott NJ, Begley DJ. Transcytosis of macromolecules at the blood-brain barrier. Adv Pharmacol. 2014;71:147–63.CrossRefPubMed
9.
Zurück zum Zitat Antonescu CN, McGraw TE, Klip A. Reciprocal regulation of endocytosis and metabolism. Cold Spring Harb Perspect Biol. 2014;6(7):a016964.CrossRefPubMed Antonescu CN, McGraw TE, Klip A. Reciprocal regulation of endocytosis and metabolism. Cold Spring Harb Perspect Biol. 2014;6(7):a016964.CrossRefPubMed
10.
Zurück zum Zitat Irannejad R, von Zastrow M. GPCR signaling along the endocytic pathway. Curr Opin Cell Biol. 2014;27:109–16.CrossRefPubMed Irannejad R, von Zastrow M. GPCR signaling along the endocytic pathway. Curr Opin Cell Biol. 2014;27:109–16.CrossRefPubMed
13.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
14.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
15.
Zurück zum Zitat Robinson MS. Forty Years of Clathrin-coated Vesicles. Traffic. 2015;16(12)1210–38. Robinson MS. Forty Years of Clathrin-coated Vesicles. Traffic. 2015;16(12)1210–38.
16.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol. 1999;15:705–32.CrossRefPubMed Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol. 1999;15:705–32.CrossRefPubMed
18.
Zurück zum Zitat McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–33.CrossRefPubMed McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–33.CrossRefPubMed
22.
24.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Schmid SL, Frolov VA. Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol. 2011;27:79–105.CrossRefPubMed Schmid SL, Frolov VA. Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol. 2011;27:79–105.CrossRefPubMed
26.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Rothman JE, Schmid SL. Enzymatic recycling of clathrin from coated vesicles. Cell. 1986;46(1):5–9.CrossRefPubMed Rothman JE, Schmid SL. Enzymatic recycling of clathrin from coated vesicles. Cell. 1986;46(1):5–9.CrossRefPubMed
28.
Zurück zum Zitat Ungewickell E, et al. Role of auxilin in uncoating clathrin-coated vesicles. Nature. 1995;378(6557):632–5.CrossRefPubMed Ungewickell E, et al. Role of auxilin in uncoating clathrin-coated vesicles. Nature. 1995;378(6557):632–5.CrossRefPubMed
29.
Zurück zum Zitat Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007;8(3):185–94.CrossRefPubMed Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007;8(3):185–94.CrossRefPubMed
32.
Zurück zum Zitat Harder T, Simons K. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr Opin Cell Biol. 1997;9(4):534–42.CrossRefPubMed Harder T, Simons K. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr Opin Cell Biol. 1997;9(4):534–42.CrossRefPubMed
33.
Zurück zum Zitat Parton RG, del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol. 2013;14(2):98–112.CrossRefPubMed Parton RG, del Pozo MA. Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol. 2013;14(2):98–112.CrossRefPubMed
34.
Zurück zum Zitat Nassar ZD, Parat MO. Cavin family: new players in the biology of caveolae. Int Rev Cell Mol Biol. 2015;320:235–305.CrossRefPubMed Nassar ZD, Parat MO. Cavin family: new players in the biology of caveolae. Int Rev Cell Mol Biol. 2015;320:235–305.CrossRefPubMed
35.
36.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
37.
Zurück zum Zitat Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol. 1994;127(5):1199–215.CrossRefPubMed Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol. 1994;127(5):1199–215.CrossRefPubMed
39.
Zurück zum Zitat 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.PubMed 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.PubMed
40.
41.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat 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). 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).
43.
Zurück zum Zitat Boucrot E, et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 2015;517(7535):460–5.CrossRefPubMed Boucrot E, et al. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 2015;517(7535):460–5.CrossRefPubMed
45.
46.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
47.
Zurück zum Zitat Frick M, et al. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol. 2007;17(13):1151–6.CrossRefPubMed Frick M, et al. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol. 2007;17(13):1151–6.CrossRefPubMed
48.
Zurück zum Zitat Mayor S, Parton RG, Donaldson JG. Clathrin-independent pathways of endocytosis. Cold Spring Harb Perspect Biol. 2014;6:6.CrossRef Mayor S, Parton RG, Donaldson JG. Clathrin-independent pathways of endocytosis. Cold Spring Harb Perspect Biol. 2014;6:6.CrossRef
49.
50.
Zurück zum Zitat Bitsikas V, Correa IR Jr, Nichols BJ. Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife. 2014;3:e03970.PubMedPubMedCentral Bitsikas V, Correa IR Jr, Nichols BJ. Clathrin-independent pathways do not contribute significantly to endocytic flux. Elife. 2014;3:e03970.PubMedPubMedCentral
51.
Zurück zum Zitat Elkin SR, et al. A systematic analysis reveals heterogeneous changes in the endocytic activities of cancer cells. Cancer Res. 2015;75(21):4640–50.CrossRefPubMedPubMedCentral Elkin SR, et al. A systematic analysis reveals heterogeneous changes in the endocytic activities of cancer cells. Cancer Res. 2015;75(21):4640–50.CrossRefPubMedPubMedCentral
52.
Zurück zum Zitat Salzman NH, Maxfield FR. Intracellular fusion of sequentially formed endocytic compartments. J Cell Biol. 1988;106(4):1083–91.CrossRefPubMed Salzman NH, Maxfield FR. Intracellular fusion of sequentially formed endocytic compartments. J Cell Biol. 1988;106(4):1083–91.CrossRefPubMed
53.
Zurück zum Zitat Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem. 1986;55:663–700.CrossRefPubMed Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem. 1986;55:663–700.CrossRefPubMed
54.
Zurück zum Zitat 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):539–43PubMed 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):539–43PubMed
55.
Zurück zum Zitat Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443(7112):651–7.CrossRefPubMed Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006;443(7112):651–7.CrossRefPubMed
58.
Zurück zum Zitat Balla T. Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci. 2005;118(Pt 10):2093–104.CrossRefPubMed Balla T. Inositol-lipid binding motifs: signal integrators through protein-lipid and protein-protein interactions. J Cell Sci. 2005;118(Pt 10):2093–104.CrossRefPubMed
60.
Zurück zum Zitat Klumperman J, Raposo G. The complex ultrastructure of the endolysosomal system. Cold Spring Harb Perspect Biol. 2014;6(10):a016857.CrossRefPubMed Klumperman J, Raposo G. The complex ultrastructure of the endolysosomal system. Cold Spring Harb Perspect Biol. 2014;6(10):a016857.CrossRefPubMed
61.
Zurück zum Zitat Schu PV, et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 1993;260(5104):88–91.CrossRefPubMed Schu PV, et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 1993;260(5104):88–91.CrossRefPubMed
62.
Zurück zum Zitat Odorizzi G, Babst M, Emr SD. Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci. 2000;25(5):229–35.CrossRefPubMed Odorizzi G, Babst M, Emr SD. Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci. 2000;25(5):229–35.CrossRefPubMed
63.
Zurück zum Zitat Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2(2):107–17.CrossRefPubMed Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2(2):107–17.CrossRefPubMed
64.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol. 1997;9(4):496–504.CrossRefPubMed Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol. 1997;9(4):496–504.CrossRefPubMed
66.
67.
68.
Zurück zum Zitat Hsu VW, Bai M, Li J. Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol. 2012;13(5):323–8.PubMed Hsu VW, Bai M, Li J. Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol. 2012;13(5):323–8.PubMed
69.
70.
Zurück zum Zitat Burd C, Cullen PJ. Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol. 2014;6:2.CrossRef Burd C, Cullen PJ. Retromer: a master conductor of endosome sorting. Cold Spring Harb Perspect Biol. 2014;6:2.CrossRef
71.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
72.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
73.
74.
75.
Zurück zum Zitat Henne WM, Stenmark H, Emr SD. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol. 2013;5:9.CrossRef Henne WM, Stenmark H, Emr SD. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol. 2013;5:9.CrossRef
78.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
79.
Zurück zum Zitat 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.PubMedPubMedCentral 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.PubMedPubMedCentral
80.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
81.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
82.
Zurück zum Zitat 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
83.
Zurück zum Zitat Cossart P, Helenius A. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol. 2014;6:8.CrossRef Cossart P, Helenius A. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol. 2014;6:8.CrossRef
84.
Zurück zum Zitat Adjei IM, Sharma B, Labhasetwar V. Nanoparticles: cellular uptake and cytotoxicity. Adv Exp Med Biol. 2014;811:73–91.CrossRefPubMed Adjei IM, Sharma B, Labhasetwar V. Nanoparticles: cellular uptake and cytotoxicity. Adv Exp Med Biol. 2014;811:73–91.CrossRefPubMed
85.
Zurück zum Zitat Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009;10(8):513–25.CrossRefPubMed Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009;10(8):513–25.CrossRefPubMed
86.
Zurück zum Zitat Seabra MC, Mules EH, Hume AN. Rab GTPases, intracellular traffic and disease. Trends Mol Med. 2002;8(1):23–30.CrossRefPubMed Seabra MC, Mules EH, Hume AN. Rab GTPases, intracellular traffic and disease. Trends Mol Med. 2002;8(1):23–30.CrossRefPubMed
87.
Zurück zum Zitat Cheng KW, et al. Emerging role of RAB GTPases in cancer and human disease. Cancer Res. 2005;65(7):2516–9.CrossRefPubMed Cheng KW, et al. Emerging role of RAB GTPases in cancer and human disease. Cancer Res. 2005;65(7):2516–9.CrossRefPubMed
89.
Zurück zum Zitat 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.CrossRefPubMed 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.CrossRefPubMed
90.
Zurück zum Zitat Esposito G, Clara AF, Verstreken P. Synaptic vesicle trafficking and Parkinson’s disease. Dev Neurobiol. 2012;72(1):134–44.CrossRefPubMed Esposito G, Clara AF, Verstreken P. Synaptic vesicle trafficking and Parkinson’s disease. Dev Neurobiol. 2012;72(1):134–44.CrossRefPubMed
92.
Zurück zum Zitat Goldenring JR. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat Rev Cancer. 2013;13(11):813–20.CrossRefPubMedPubMedCentral Goldenring JR. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat Rev Cancer. 2013;13(11):813–20.CrossRefPubMedPubMedCentral
93.
Zurück zum Zitat Gauthier NC, Masters TA, Sheetz MP. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 2012;22(10):527–35.CrossRefPubMed Gauthier NC, Masters TA, Sheetz MP. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 2012;22(10):527–35.CrossRefPubMed
94.
Zurück zum Zitat Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6(11):a022616.CrossRefPubMed Wandinger-Ness A, Zerial M. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol. 2014;6(11):a022616.CrossRefPubMed
Metadaten
Titel
Endocytic pathways and endosomal trafficking: a primer
verfasst von
Sarah R. Elkin
Ashley M. Lakoduk
Sandra L. Schmid, PhD
Publikationsdatum
01.05.2016
Verlag
Springer Vienna
Erschienen in
Wiener Medizinische Wochenschrift / Ausgabe 7-8/2016
Print ISSN: 0043-5341
Elektronische ISSN: 1563-258X
DOI
https://doi.org/10.1007/s10354-016-0432-7

Weitere Artikel der Ausgabe 7-8/2016

Wiener Medizinische Wochenschrift 7-8/2016 Zur Ausgabe