Skip to main content
SpringerLink
Log in

On vesicles and membrane compartments

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Two different mechanisms have been proposed to explain transport along the endocytic and biosynthetic transport routes in cells. The first involves stable compartments connected by vesicular traffic while the second argues that the key organelles (early endosomes or the cis Golgi) form de novo by fusion of vesicles and subsequently mature into later forms. In the first part of this article, I propose a classification that distinguishes between stable, preexisting membrane compartments and vesicles that are, by definition, transient organelles. In this scheme, compartments, but not vesicles, are capable of homotypic fusion while vesicles, but not compartments, are able to “mature”, a process defined as an irreversible set of biochemical events which lead to a physiologically distinct end-state of the vesicle prior to its vectorial fusion with a target compartment. In the second part, I summarize my current ideas about the ultrastructural organization of the ER-Golgi region. Finally, I review the cell biology of selected examples of different vesicle types in order to exemplify the fascinating diversity of functions that this class of membrane organelles has evolved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

COP:

coatomer

ECV:

endosome carrier vesicle

ER:

endoplasmic reticulum

HRP:

horseradish peroxidase

IC:

intermediate compartment between ER and Golgi

MVB:

multivesicular body

NSF:

N-ethyl maleimide sensitive factor

SNAPS:

soluble NSF associated proteins

TGN:

trans Golgi network

References

  • Almers W (1994) How fast can you get? Nature 367: 682–684

    Google Scholar 

  • Alquier C, Guenin P, Munari-Silem Y, Audebet C, Rousset B (1988) Isolation of pig thyroid lysosomes. Biochem J 232: 529–537

    Google Scholar 

  • Anderson RGW, Brown MS, Goldstein JL (1977) Role of the coated endocytic vesicle in the uptake of receptor bound low density lipoprotein in human fibroblasts. Cell 10: 351–364

    Google Scholar 

  • Aniento F, Emans N, Griffiths G, Gruenberg J (1993) Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol 123: 1373–1387

    Google Scholar 

  • Baggiolini M, Horisberger U, Gennaro R, Dewald B (1985) Identification of three types of granules in neurophils of ruminants. Lab Invest 52: 151

    Google Scholar 

  • Bainton DF, Farquhar MG (1970) Segregation and packaging of granule enzymes in eosinophilic leukocytes. J Cell Biol 45: 54–73

    Google Scholar 

  • Bajjalieh S, Scheller RH (1993) The biochemistry of neurotransmitter secretion. J Biol Chem 5: 1971–1974

    Google Scholar 

  • Balch WE, Mccaffery JM, Plutner H, Farquhar MG (1994) Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 76: 841–852

    Google Scholar 

  • Baron W, Alvarez-Dominquez C, Mayorga L, Stahl PD (1995) Membrane trafficking along the phagocytotic pathway. Trends Cell Biol 5: 100–104

    Google Scholar 

  • Bauernfeind R, Regnier-Vigouroux A, Flatmark T, Huttner WB (1993) Selective storage of acetylcholine, but not catecholamines in neuroendocrine synapse-like microvesicles of early endosomal origin. Neuron 11: 105–121

    Google Scholar 

  • Becker B, Bölinger B, Melkonian M (1995) Anterograde transport of algal scales through the Golgi complex is not mediated by vesicles. Trends Cell Biol 5: 305–307

    Google Scholar 

  • Berthiaume EP, Medina C, Swanson JA (1995) Molecular size-fractionation during endocytosis in macrophages. J Cell Biol 129: 989–998

    Google Scholar 

  • Blocker A, Severin FF, Haberman A, Hyman AA, Griffiths G, Burkhardt JK (1995) Map-dependent binding of phagosomes to microtubules. J Biol Chem 271: 3803–3811

    Google Scholar 

  • Bomsel M, Prydz K, Parton RG, Gruenberg J, Simons K (1989) Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol 109: 3243–3258

    Google Scholar 

  • —, Parton R, Kuznetsov SA, Schroer TA, Gruenberg J (1992) Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 62: 719–731

    Google Scholar 

  • Breckenridge LJ, Almers W (1987) Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328: 814–817

    Google Scholar 

  • Bretz U, Baggiolini M (1974) Biochemical and morphological characterization of azurophil and specific granules of human neutrophilic polymorphonuclear leukocytes. J Cell Biol 63: 251–269

    Google Scholar 

  • Brown RM Jr, Romanovicz DK (1976) Biogenesis and structure of Golgi-derived cellulosic scales inPleurochrysis. 1. Role of the endomembrane system in scale assembly and exocytosis. Appl Polymer Symp 28: 537–585

    Google Scholar 

  • Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715–728

    Google Scholar 

  • Burgoyne RD, Morgan A (1993) Regulated exocytosis. Biochem J 293: 305–316

    Google Scholar 

  • — — (1995) Ca2+ and secretory vesicle dynamics. Trends Neurosci 18: 191–196

    Google Scholar 

  • Burkhardt JK, Hester S, Lapham CK, Argon Y (1990) The lytic granules of natural killer cells are dual-function organelles combining secretory and pre-lysosomal compartments. J Cell Biol 111: 2327–2340

    Google Scholar 

  • —, Mcilvain JM Jr, Sheetz MP, Argon Y (1993) Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro. J Cell Sci 104: 151–162

    Google Scholar 

  • Chamberlain H, Roth D, Morgan A, Burgoyne RD (1995) Distinct effects of α-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. J Cell Biol 130: 1063–1070

    Google Scholar 

  • Chanock ST, El Penna J, Smith RM, Babior M (1994) The respiratory burst oxidase. J Biol Chem 269: 24519–24522

    Google Scholar 

  • Clague M, Urbé S, Aniento F, Gruenberg J (1994) Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 269: 21–24

    Google Scholar 

  • Claude A (1970) Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. J Cell Biol 47: 745–766

    Google Scholar 

  • Clermont Y, Rambourg A, Hermo L (1994) Connections between the various elements of the cis- and mid-compartments of the Golgi apparatus of early rat spermatids. Anat Rec 240: 469–480

    Google Scholar 

  • Cole NB, Lippincott-Schwarz J (1995) Organization of organelles and membrane traffic by microtubules. Curr Opin Cell Biol 7: 55–64

    Google Scholar 

  • Cooper MS, Cornell-Bell AH, Chernjavsky A, Dani WJ, Smith SJ (1988) Tubulovesicular processes emerge from the trans-Golgi cisternae, extended along microtubules and interlink adjacent trans-Golgi elements into a reticulum. Cell 62: 135–145

    Google Scholar 

  • Cudmore S, Cossart P, Griffiths G, Way M (1995) Actin-based motility of vaccinia virus. Nature 378: 636–638

    Google Scholar 

  • Dahl R, Staehelin LA (1989) High-pressure freezing for the preservation of biological structure: theory and practice. J Electron Microsc Tech 13: 165–174

    Google Scholar 

  • Dauwalder M, Whalley WG, Starr RC (1980) Differentiation and secretion inVolvox. J Ultrastruct Res 70: 318–335

    Google Scholar 

  • DeCamilli P, Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52: 625–645

    Google Scholar 

  • Deng YP, Griffiths G, Storrie B (1991) Comparative behavior of lysosomes and the pre-lysosome compartment (PLC) in vivo cell fusion experiments. J Cell Sci 99: 571–582

    Google Scholar 

  • Desjardins M (1995) The kiss and run hypothesis of phagosome maturation. Trends Cell Biol 5: 183–186

    Google Scholar 

  • —, Celis JE, Van Meer G, Dieplinger H, Jahraus A, Griffiths G, Huber LA (1994a) Molecular characterization of phagosomes. J Biol Chem 269: 32194–32200

    Google Scholar 

  • —, Huber LA, Parton RG, Griffiths G (1994b) Biogenesis of phagosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124: 677–688

    Google Scholar 

  • Desnos C, Clift-O'Grady L, Kelly RB (1995) Biogenesis of synaptic vesicles in vitro. J Cell Biol 130: 1041–1049

    Google Scholar 

  • Detilleux PG, Deyoe BL, Cheville NF (1990) Penetration and intracellular growth ofBrucella abortus in non-phagocytic cells in vitro. Infect Immun 58: 2320–2328

    Google Scholar 

  • Doms RW, Russ G, Yewdell JW (1989) Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J Cell Biol 109: 61–72

    Google Scholar 

  • Falkow S, Isberg RR, Portnoy DA (1992) The interaction of bacteria with mammalian cells. Annu Rev Cell Biol 8: 333–363

    Google Scholar 

  • Farquhar MG, Palade GE (1981) The Golgi apparatus (complex) (1954–1981) from artifact to center stage. J Cell Biol 91: 77–103

    Google Scholar 

  • Felder S, Miller K, Moehren G, Ullrich A, Schlessinger J, Hopkins CR (1990) Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61: 623–634

    Google Scholar 

  • Ferro-Novick S, Jahn R (1994) Vesicle fusion from yeast to man. Nature 370: 191–193

    Google Scholar 

  • —, Novick P (1993) The role of GTP-binding proteins in transport along the exocytic pathway. Annu Rev Cell Biol 9: 575–599

    Google Scholar 

  • Finlay BB, Falcow S (1990) Invasion of cells by microorganisms. J Infect Dis 162: 1096–1106

    Google Scholar 

  • Forgac M, Cantley L, Wiedenmann B, Altstiel L, Branton D (1983) Clathrin-coated vesicles contain an ATP-dependent proton pump. Proc Natl Acad Sci USA 80: 1300–1303

    Google Scholar 

  • Gennaro R, Dewald B, Horisberger U, Gubler HU, Baggiolini M (1983) A novel type of cytoplasmic granule in bovine neutrophils. J Cell Biol 96: 1651–1661

    Google Scholar 

  • Geuze HJ, Stoorvogel W, Strous GJ, Slot JW, Bleekemolen JE, Mellman I (1988) Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J Cell Biol 107: 2491–2501

    Google Scholar 

  • Griffing LR (1991) Comparisons of Golgi structures and dynamics in plant and animal cells. J Electron Microsc Tech 17: 179–199

    Google Scholar 

  • Griffiths G (1993) Fine structure immunocytochemistry. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • —, Gruenberg J (1991) The arguments for pre-existing early and late endosomes. Trends Cell Biol 1: 5–9

    Google Scholar 

  • —, Simons K (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234: 438–443

    Google Scholar 

  • —, Rottier PJM (1992) Cell biology of viruses that assemble along the biosynthetic pathway. Semin Cell Biol 3: 367–381

    Google Scholar 

  • —, Quinn P, Warren G (1983) Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J Cell Biol 96: 835–850

    Google Scholar 

  • —, Hoflack B, Simons K, Mellman I, Kornfeld S (1988) The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52: 329–341

    Google Scholar 

  • —, Back R, Marsh M (1989) A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J Cell Biol 109: 2703–2720

    Google Scholar 

  • —, Matteoni R, Back R, Hoflack B (1990a) Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J Cell Sci 95: 441–461

    Google Scholar 

  • —, Hollinshead R, Hemmings BA, Nigg EA (1990b) Ultrastructural localization of the regulatory (RII) subunit of cyclic AMP-dependent protein kinase to subcellular compartments active in endocytosis and recycling of membrane receptors. J Cell Sci 96: 691–703

    Google Scholar 

  • —, Parton RG, Lucocq J, van Deurs B, Brown D, Slot JW, Geuze HJ (1993) The immunofluorescent era of membrane traffic. Trends Cell Biol 3: 214–219

    Google Scholar 

  • —, Ericsson M, Krijnse-Locker J, Nilsson T, Goud B, Soeling H-D, Tang BL, Wong SH, Hong W (1994) Localization of the KDEL receptor to the Golgi complex and the intermediate compartment in mammalian cells. J Cell Biol 127: 1557–1574

    Google Scholar 

  • Gruenberg J, Clague M (1992) Regulation of intracellular membrane transport. Curr Opin Cell Biol 4: 593–599

    Google Scholar 

  • —, Howell KE (1989) Membrane traffic in endocytosis: insights from cell-free assays. Annu Rev Cell Biol 5: 453–481

    Google Scholar 

  • —, Griffiths G, Howell KE (1989) Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 108: 1301–1316

    Google Scholar 

  • Hansen SH, Sandvig K, van Deurs B (1991) The preendosomal compartment comprises distinct coated and noncoated endocytic vesicle populations. J Cell Biol 113: 731–741

    Google Scholar 

  • Hauri HP, Schweizer A (1992) The endoplasmic reticulum-Golgi intermediate compartment. Curr Opin Cell Biol 4: 600–608

    Google Scholar 

  • Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57: 315–344

    Google Scholar 

  • Ho WC, Allan VJ, Van Meer G, Berger EG, Kreis TE (1989) Reclustering of scattered golgi elements occurs along microtubules. Eur J Cell Biol 48: 250–263

    Google Scholar 

  • Huttner WB, Tooze SA (1989) Biosynthetic protein transport in the secretory pathway. Curr Opin Cell Biol 1: 648–654

    Google Scholar 

  • Jamieson JD, Palade GE (1967) Intracellular transport of secretory proteins in the pancreatic exocrine cell. Role of peripheral elements of the Golgi complex. J Cell Biol 34: 597–615

    Google Scholar 

  • Jessel TM, Kandel ER (1993) Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell 72: 1–30

    Google Scholar 

  • Joiner KA, Dubremetz JF (1993) Toxoplasma gondii: a protozoan for the nineties. Infect Immun 61: 1169–1172

    Google Scholar 

  • Kelly RB (1990) Microtubules, membrane traffic, and cell organization. Cell 61: 5–7

    Google Scholar 

  • — (1991) Secretory granule and synaptic vesicle formation. Curr Opin Cell Biol 3: 654–660

    Google Scholar 

  • — (1993) Storage and release of neurotransmitters. Neuron 10: 45–53

    Google Scholar 

  • Killisch I, Steinlein P, Römisch K, Hollinshead R, Beug H, Griffiths G (1992) Characterization of early and late endocytic compartments of the transferrin cycle. J Cell Sci 103: 211–232

    Google Scholar 

  • Knapp PE, Swanson JA (1990) Plasticity of the tubular lysosome compartment in macrophages. J Cell Sci 95: 433–439

    Google Scholar 

  • Kornfeld S, Mellman I (1989) The biogenesis of lysosomes. Annu Rev Cell Biol 5: 482–525

    Google Scholar 

  • Krijnse-Locker J, Ericsson M, Rottier PJM, Griffiths G (1994) Characterization of the budding compartment of mouse hepatitis virus. J Cell Biol 124: 55–70

    Google Scholar 

  • —, Parton RG, Fuller SD, Griffiths G, Dotti C (1995) The organization of the endoplasmic reticulum and the intermediate compartment in cultured hippocampal neurons. Mol Biol Cell 6: 1315–1332

    Google Scholar 

  • Latterich M, Schekman R (1994) The karyogamy gene KAR2 and novel proteins are required for ER-membrane fusion. Cell 78: 87–98

    Google Scholar 

  • —, Fröhlich K-U, Schekman R (1995) Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 82: 885–893

    Google Scholar 

  • Lee C, Bo Chen Lan (1988) Dynamic behavior of endoplasmic reticulum. Cell 54: 37–46

    Google Scholar 

  • Lindsey JD, Ellisman MH (1985a) The neuronal endomembrane system. Direct links between rough endoplasmatic reticulum and thecis elements of the Golgi apparatus. J Neurosci 5: 3111–3123

    Google Scholar 

  • — — (1985b) The neuronal endomembrane system. The multiple forms of the Golgi apparatuscis element. J Neurosci 5: 3124–3134

    Google Scholar 

  • Lippincott-Schwarz J, Yuan LC, Bonifacino JS, Klausner RD (1989) Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56: 801–813

    Google Scholar 

  • Lollike K, Borregaard N, Lindau M (1995) The exocytic fusion pore of small granules has a conductance similar to an ion channel. J Cell Biol 129: 99–104

    Google Scholar 

  • Ludwig T, Griffiths G, Hoflack B (1991) Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J Cell Biol 115: 1561–1572

    Google Scholar 

  • McDowall A, Gruenberg J, Romisch K, Griffiths G (1989) The structure of organelles of the endocytic pathway in hydrated cryosections of cultured cells. Eur J Cell Biol 49: 281–294

    Google Scholar 

  • McKanna JA, Haigler HT, Cohen S (1979) Hormone receptor topology and dynamics: morphological analysis using ferritinlabelled epidermal growth factor. Proc Natl Acad Sci USA 76: 5689–5693

    Google Scholar 

  • Melkonian M, Becker B, Becker D (1991) Scale formation in algae. J Electron Microsc Tech 17: 165–178

    Google Scholar 

  • Mellman I, Simons K (1992) The Golgi complex: in vitro veritas? Cell 68: 829–840

    Google Scholar 

  • Monck JR, Alvarez de Toledo G, Fernandez JM (1990) Tension in secretory granule membranes causes extensive membrane transfer through the exocytic fusion pore. Proc Natl Acad Sci USA 87:7804–7808

    Google Scholar 

  • Morel F, Doussire J, Vignais P (1991) The superoxide-generating oxidase of phagocytic cells. Eur J Biochem 201: 523–546

    Google Scholar 

  • Morré DJ, Kartenbeck J, Franke WW (1979) Membrane flow and interconversions among endomembranes. Biochim Biophys Acta 559: 71–105

    Google Scholar 

  • Muallem S, Kwiatkowska K, Xu X, Yin HL (1995) Actin filament is a sufficient final trigger for exocytosis in nonexitable cells. J Cell Biol 128: 589–598

    Google Scholar 

  • Mullock BM, Perez JH, Kuwana T, Gray SR, Luzio JP (1994) Lysosomes can fuse with late endosomes in a cell-free system from rat liver. J Cell Biol 126: 1173–1182

    Google Scholar 

  • Murphy RF (1991) Maturation models for endosome and lysosome biogenesis. Trends Cell Biol 1: 77–82

    Google Scholar 

  • Oprins A, Duden R, Kreis TE, Geuze HJ, Slot JW (1993) Beta-COP localizes mainly to the cis-Golgi side in exocrine pancreas. J Cell Biol 121: 49–59

    Google Scholar 

  • Orci L, Ravazzola M, Amherdt M, Madsen O, Vassali J-D, Perrelet A (1985) Direct identification of prohormone conversion site in insulin-secreting cells. Cell 42: 671–681

    Google Scholar 

  • Paiement J, Beaufay H, Godelaine D (1980) Coalescence of microsomal vesicles from rat liver: a phenomenon occurring in parallel with enhancement of the glycosylation activity during incubation of stripped rough microsomes with GTP. J Cell Biol 86: 29–37

    Google Scholar 

  • Palade GE (1975) Intracellular aspects of the process of protein secretion. Science 189: 347–358

    Google Scholar 

  • — (1983) Membrane biogenesis: an overview. Methods Enzymol 96: XXIX-LV

    Google Scholar 

  • Parton RG (1991) Endocytosis in polarized cells. Semin Cell Biol 2: 387–395

    Google Scholar 

  • —, Prydz K, Bomsel M, Simons K, Griffiths G (1989) Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J Cell Biol 109: 3259–3272

    Google Scholar 

  • —, Simons K, Dotti CG (1992) Axonal and dendritic endocytic pathways in cultured neurons. J Cell Biol 119: 123–137

    Google Scholar 

  • Pelham HRB (1994) About turn for the COPs. Cell 79: 1125–1127

    Google Scholar 

  • Peters PJ, Borst J, Oorschot V, Fukuda M, Krahenbuhl O, Tschopp J, Slot JW, Geuze HJ (1991) Cytotoxic T lymphocyte granules are secretory lysosomes containing both perform and granzymes. J Exp Med 173: 1099–1109

    Google Scholar 

  • Pierre P, Scheel J, Rickard JE, Kreis TE (1992) CLIP-170 links endocytic vesicles to microtubules. Cell 70: 887–900

    Google Scholar 

  • Pitt A, Mayorga LS, Schwartz AL, Stahl PD (1992) Transport of phagosomal components to an endosomal compartment. J Biol Chem 267: 126–142

    Google Scholar 

  • Rabinowitz S, Horstmann H, Gordon S, Griffiths G (1992) Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J Cell Biol 116: 95–112

    Google Scholar 

  • Raposo G, van Santen HM, Leijendekker R, Geuze HJ, Ploegh HL (1995) Misfolded major histocompatibility complex class I molecules accumulate in an expanded ER-Golgi intermediate compartment. J Cell Biol 131: 1403–1420

    Google Scholar 

  • Record RD, Griffing LR (1988) Convergence of the endocytic and lysosomal pathways in soybean protoplasts. Planta 176: 425–432

    Google Scholar 

  • Robinson DG, Kristen U (1982) Membrane flow via the Golgi apparatus of higher plant cells. Int Rev Cytol 27: 89–125

    Google Scholar 

  • Robinson MR, Badwey JA (1995) The NADPH oxidase complex of phagocytic leukocytes: a biochemical and cytochemical view. Histochemistry 103: 163–180

    Google Scholar 

  • Rodriquez L, Stirling CJ, Woodman PG (1993) Multiple N-ethylmaleimide-sensitive components are required for endosomal vesicle fusion. Mol Biol Cell 5: 773–783

    Google Scholar 

  • Rome LH, Cairn LR (1981) Degradation of mucopolysaccharide in intact isolated lysosomes. J Biol Chem 256: 10763–10768

    Google Scholar 

  • Roos N, Cyrklaff M, Cudmore S, Blasco R, Krijnse-Locker J, Griffiths G (1996) A novel immunogold cryo EM method to investigate the structure of the IMV/EEV. EMBO J 15: 2343–2355

    Google Scholar 

  • Rothman JE (1981) The Golgi apparatus: two organelles in tandem. Science 213: 1212–1219

    Google Scholar 

  • —, Orci L (1992) Molecular dissection of the secretory pathway. Nature 355: 409–415

    Google Scholar 

  • —, Warren G (1994) Implication of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 4: 220–223

    Google Scholar 

  • Russell DG (1995) Mycobacterium and Leishmania: stowaways in the endosomal network. Trends Cell Biol 5: 125–128

    Google Scholar 

  • Saraste J, Kuismanen E (1992) Pathways of protein sorting and membrane traffic between the rough endoplasmic reticulum and the Golgi complex. Semin Cell Biol 3: 343–355

    Google Scholar 

  • Schekman RW (1992) Genetic and biochemical analysis of vesicular traffic in yeast. Curr Opin Cell Biol 4: 587–592

    Google Scholar 

  • Schwarz H, Humbel BM (1989) Influence of fixatives and embedding media on immunolabelling of freeze-substituted cells. Scanning Microsc Suppl 3: 57–64

    Google Scholar 

  • Segal AW, Dorling J, Coade S (1980) Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. J Cell Biol 85: 42–50

    Google Scholar 

  • —, Geisow M, Garcia R, Harper A, Miller R (1981) The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 290: 406–409

    Google Scholar 

  • Selsted ME, Ouellette AJ (1995) Defensins in granules of phagocytic and non-phagocytic cells. Trends Cell Biol 5: 114–119

    Google Scholar 

  • Sesso A, de Faria FP, Iwamura ES, Correa H (1994) A three-dimensional reconstruction study of the rough ER-Golgi interface in serial thin sections of the pancreatic acinar cell of the rat. J Cell Sci 107: 517–528

    Google Scholar 

  • Silverstein SC, Greenberg S, Di Virgilio F, Steinberg TH (1989) Phagocytosis. In: Paul WE (ed) Fundamental immunology. Raven, New York, pp 703–720

    Google Scholar 

  • Sodeik B, Doms RW, Ericsson M, Hiller G, Machamer CE, van't Hof W, van Meer G, Moss B, Griffiths G (1993) Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J Virol 69: 3560–3574

    Google Scholar 

  • Sontag J-M, Aunis D, Bader M-F (1988) Peripheral actin filaments control calcium-mediated catecholamine release from streptolysin-O-permeabilized chromaffin cells. J Cell Biol 46: 316–326

    Google Scholar 

  • Staehelin LA, Moore I (1995) The plant Golgi apparatus: structure, functional-organisation and trafficking mechanisms. Annu Rev Plant Physiol Plant Mol Biol 46: 261–288

    Google Scholar 

  • Stieber A, Erulkar SD, Gonatas NK (1989) A hypothesis for the superior sensitivity of wheat germ agglutinin as a neuroanatomical probe. Brain Res 495: 131–139

    Google Scholar 

  • Stinchcombe JC, Nomoto H, Cutler DF, Hopkins CR (1995) Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J Cell Biol 131: 1387–1401

    Google Scholar 

  • Storrie B (1988) Assembly of lysosomes: perspectives from comparative molecular cell biology. Int Rev Cytol 111: 53–105

    Google Scholar 

  • Studer D, Michel M, Müller M (1989) High-pressure freezing comes of age. Scanning Microsc Suppl 3: 253–269

    Google Scholar 

  • Südhof TC, De Camilli P, Niemann H, Jahn R (1993) Membrane fusion machinery: insights from synaptic proteins. Cell 75: 1–4

    Google Scholar 

  • Swanson J, Watts C (1995) Macropinocytosis. Trends Cell Biol 5: 424–428

    Google Scholar 

  • —, Burke E, Silverstein SC (1987) Tubular lysosomes accompany stimulated pinocytosis in macrophages. J Cell Biol 104: 1217–1222

    Google Scholar 

  • Tanchak MA, Fowke LC (1987) The morphology of multivesicular bodies in soybean protoplasts and their role in endocytosis. Protoplasma 138: 173–182

    Google Scholar 

  • Tooze SA, Tooze J, Warren G (1988) Site of addition of N-acetylgalactosamine to the El glycoprotein of mouse hepatitis virus-A59. J Cell Biol 106: 1475–1487

    Google Scholar 

  • —, Kern HF, Fuller SD, Howell KE (1989) Condensation-sorting events in the rough endoplasmic reticulum of exocrine pancreatic cells. J Cell Biol 109: 35–50

    Google Scholar 

  • Van Deurs B, Petersen OW, Bundgaard M (1984) Identification of free coated pinocytic vesicles in Swiss 3T3 cells. EMBO J 3: 1959–1964

    Google Scholar 

  • —, Holm PK, Kayser L, Sandvig K, Hansen SH (1993) Multivesicular bodies in hep-2 cells are maturing endosomes. Eur J Cell Biol 61: 208–224

    Google Scholar 

  • Voorhout WF, Veenendaal T, Kuroki Y, Ogasawara Y, van Golde LMG, Geuze HJ (1992a) Immunocytochemical localization of surfactant protein-d (sp-d) in type-II cells, clara cells, and alveolar macrophages of rat lung. J Histochem Cytochem 40: 1589–1597

    Google Scholar 

  • — —, Haagsman P, Weaver TE, Whitsett JA, Geuze HJ (1992b) Intracellular processing of pulmonary surfactant protein-b in an endosomal/lysosomal compartment. Am J Physiol 263: L479–486

    Google Scholar 

  • Wall DA, Wilson G, Hubbard AL (1980) The galactose-specific recognition system of mammalian liver: the route of ligand internalization in rat hepatocytes. Cell 21: 79–93

    Google Scholar 

  • Warren G (1993) Membrane partitioning during cell division. Annu Rev Biochem 62: 323–348

    Google Scholar 

  • Wileman T, Harding C, Stahl P (1985) Receptor-mediated endocytosis. Biochem J 232: 1–14

    Google Scholar 

  • Xu H, Shields D (1994) Prosomatostatin processing in permeabilized cells. J Biol Chem 269: 22875–22881

    Google Scholar 

  • Zachgo S, Dobberstein B, Griffiths G (1992) A block in degradation of MHC-class II-associated invariant chain associated with a reduction in transport from endosome carrier vesicles to the prelysosome compartment. J Cell Sci 103: 811–822

    Google Scholar 

  • Zanetti M, Litteri L, Gennaro R, Horstmann H, Romeo D (1990) Bactenecins, defense polypeptides of bovine neutrophils are generated from precursor molecules stored in the large granules. J Cell Biol 111: 1363–1371

    Google Scholar 

  • Zerial M, Stenmark H (1993) Rab GTPases in vesicular transport. Curr Opin Cell Biol 5: 613–620

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. European Molecular Biology Laboratory, Meyerhofstrasse 1, D-69012, Heidelberg, Federal Republic of Germany

    Gareth Griffiths

Authors
  1. Gareth Griffiths
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to Professor Eldon H. Newcomb in recognition of his contributions to cell biology

Rights and permissions

Reprints and permissions

About this article

Cite this article

Griffiths, G. On vesicles and membrane compartments. Protoplasma 195, 37–58 (1996). https://doi.org/10.1007/BF01279185

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01279185

Keywords

Search

Navigation