Secretory Lysosomes and the Production of Exosomes

  • Chapter
Unusual Secretory Pathways: From Bacteria to Man

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

Eukaryotic cells secrete proteins either by the so-called constitutive secretion involving vesicular transport and exocytosis or by the regulated secretion of storage granules upon proper stimulation.1,2 Only recently has one become aware that alternative mechanisms operate that may account for the secretion of specific membrane and cytotoxic proteins. Indeed, accumulating evidence indicates that cellular compartments displaying intralumenal membrane vesicles, collectively named multivesicular bodies (MVBs), fuse with the plasma membrane in an exocytic manner. During exocytosis, the 60 to 80 nm membrane vesicles present in the lumen of MVBs are released into the extracellular environment. The secreted membrane vesicles are called exosomes.3–6

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

eBook
USD 9.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. Palade G. Intracellular aspects of the process of protein secretion. Science 1975; 189: 347–385.

    PubMed  CAS  Google Scholar 

  2. Burgess TL, Kelly RB. Constitutive and regulated secretion of proteins. Ann Rev Cell Biol 1987; 3: 243–93.

    PubMed  CAS  Google Scholar 

  3. Pan BT, Teng K, Wu C et al. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 1985; 101: 942–948.

    PubMed  CAS  Google Scholar 

  4. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983; 97: 329–339.

    PubMed  CAS  Google Scholar 

  5. Vidal M, Sainte-Marie J, Philippot JR et al. Asymmetric distribution of phospholipids in the membrane of vesicles released during in vitro maturation of guinea pig reticulocytes: evidence precluding a role for “aminophospholipid translocase”. J Cell Physiol 1989; 140: 455–62.

    PubMed  CAS  Google Scholar 

  6. Raposo G, Nijman HW, Stoorvogel W et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996; 183: 1161–1172.

    PubMed  CAS  Google Scholar 

  7. Harding CV, Levy M, Stahl P. Morphological analysis of ligand uptake and processing: the role of multivesicular endosomes and CURL in receptor-ligand processing. Eur J Cell Biol 1985; 36: 230–238.

    PubMed  CAS  Google Scholar 

  8. van Deurs B, Holm PK, Kayser L et al. Multivesicular bodies in HEp-2 cells are maturating endosomes. Eur J Cell Biol 1993; 61: 208–224.

    PubMed  Google Scholar 

  9. Trowbridge IS, Collawn JF, Hopkins CR. Signal-dependent membrane protein trafficking in the endocytic pathway. Ann Rev Cell Biol 1993; 9: 129–161.

    PubMed  CAS  Google Scholar 

  10. Kornfeld S, Mellman I. The biogenesis of lysosomes. Ann Rev Cell Biol 1989; 5: 483–525.

    PubMed  CAS  Google Scholar 

  11. Hunziker W, Geuze HJ. Intracellular trafficking of lysosomal membrane proteins. BioEssays 1996; 18: 379–389.

    PubMed  CAS  Google Scholar 

  12. Griffiths GM. Secretory lysosomes-a special mechanism of regulated secretion in haematopoietic cells. Trends Cell Biol 1996; 6: 329–332.

    PubMed  CAS  Google Scholar 

  13. Peters PJ, Geuze HJ, van der Donk HA et al. Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur J Immunol 1989; 19: 1469–1475.

    PubMed  CAS  Google Scholar 

  14. Peters PJ, Borst J, Oorschot V et al. Cytotoxic lymphocyte-T granules are secretory lysosomes, containing both perforin and granzymes. J Exp Med 1991; 173: 1099–1109.

    PubMed  CAS  Google Scholar 

  15. Burkhardt JK, Hester S, Lapham CK et al. The lytic granules of natural killer cells are dual-function organelles combining secretory and prelysosomal compartments. J Cell Biol 1990; 111: 2327–2340.

    PubMed  CAS  Google Scholar 

  16. Dvorak AM. Ultrastructural analysis of human mast cells and basophils. In: Marone G, ed. Human basophils and mast cells. Chem Immunol Basel, Karger: 1995: 1–33. vol 61).

    Google Scholar 

  17. Chi EY, Lagunoff D. Abnormal mast cell granules in the beige (ChediakHigashi syndrome) mouse. J Histochem Cytochem 1975; 23: 117–122.

    PubMed  CAS  Google Scholar 

  18. Parmley RT, Poon MC, Crist WM, Malluh A. Giant platelet granules in a child with the Chediak-Higashi syndrome. Am J Hematol 1979; 6: 51–60.

    PubMed  CAS  Google Scholar 

  19. White JG, Clawson CC. The Chediak-Higashi syndrome; the nature of the giant neutrophil granules and their interactions with cytoplasm and foreign particulates. Progressive enlargement of the massive inclusions in mature neutrophils. Am J Pathol 1980; 98: 151–196.

    PubMed  CAS  Google Scholar 

  20. Harding C, Heuser J, Stahl P. Endocytosis and intracellular processing of transferrin and colloidal-gold transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur J Cell Biol 1984; 35: 256–263.

    PubMed  CAS  Google Scholar 

  21. Johnstone RM, Adam M, Hammond JR et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987; 262: 9412–9420.

    PubMed  CAS  Google Scholar 

  22. Vidal M, Stahl PD. The small GTP-binding proteins Rab 4 and ARF are associated with released exosomes during reticulocyte maturation. Eur J Cell Biol 1993; 60: 261–267.

    PubMed  CAS  Google Scholar 

  23. Griffiths GM. The cell biology of CTL killing. Curr Opin Immunol 1995; 7: 343–348.

    PubMed  CAS  Google Scholar 

  24. Peters P, Geuze HJ, van der Donk HA et al. A new model for lethal hit delivery by cytotoxic T lymphocytes. Immunol Today 1990; 11: 28–32.

    PubMed  CAS  Google Scholar 

  25. Gruenberg J, Howell KE. Membrane traffic in endocytosis: insights from cell-free systems. Ann Rev Cell Biol 1989; 5: 453–481.

    PubMed  CAS  Google Scholar 

  26. Hopkins CR, Trowbridge IS. Internalization and processing of transfer-rin and transferrin receptors in human carcinoma cells. J Cell Biol 1983; 97: 508–521.

    PubMed  CAS  Google Scholar 

  27. Geuze HJ, Slot JW, Strous GJ et al. Intracellular site of asialoglycoprotein receptor-ligand uncoupling: double label immunoelectron microscopy during receptor-mediated endocytosis. Cell 1983; 32: 277–287.

    PubMed  CAS  Google Scholar 

  28. Geuze HJ, Slot JW, Schwartz AL. Membranes of sorting organelles display lateral heterogeneity in receptor distribution. J Cell Biol 1987; 104: 1715–1723.

    PubMed  CAS  Google Scholar 

  29. Tooze J, Hollinshead M. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 1991; 115: 635–653.

    PubMed  CAS  Google Scholar 

  30. van Deurs B, Petersen OW, Olsnes S et al. The ways of endocytosis. Int Rev Cytol 1989; 117: 131–177.

    PubMed  Google Scholar 

  31. Courtoy PJ. Dissection of endosomes. In: JC Steer JH, ed. Trafficking of Membrane Proteins. New York: 1991: 103–156.

    Google Scholar 

  32. Goldstein JL, Brown MS, Anderson RGW et al. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Ann Rev Cell Biol 1985; 1: 1–39.

    PubMed  CAS  Google Scholar 

  33. Stoorvogel W, Geuze HJ, Strous GJ. Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J Cell Biol 1987; 104: 1261–1268.

    PubMed  CAS  Google Scholar 

  34. Stoorvogel W, Geuze HJ, Griffith TM et al. Relations between the intracellular pathways of the receptors for transferrin, asialoglycoprotein, and mannose 6-phosphate in human hepatoma cells. J Cell Biol 1989; 108: 2137–2148.

    PubMed  CAS  Google Scholar 

  35. Dunn KW, McGraw TE, Maxfield FR. Interactive fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J Cell Biol 1989; 109: 3303–3014.

    PubMed  CAS  Google Scholar 

  36. Hopkins CR, Gibson A, Shipman M et al. In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J Cell Biol 1994; 125: 1265–1274.

    PubMed  CAS  Google Scholar 

  37. Gosh RN, Maxfield FR. Evidence for nonvectorial, retrograde transfer-rin trafficking in the early endosomes of HEp2 cells. J Cell Biol 1995; 128: 549–561.

    Google Scholar 

  38. Stoorvogel W, Oorschot V, Geuze HJ. A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 1996; 132: 21–33.

    PubMed  CAS  Google Scholar 

  39. Griffiths G, Gruenberg J. The arguments of pre-existing early and late endosomal compartments. Trends Cell Biol 1991; 1: 5–9.

    PubMed  CAS  Google Scholar 

  40. Roederer M, Barry JR, Wilson RB et al. Endosomes can undergo an ATP-dependent density increase in the absence of dense lysosomes. Eur J Cell Biol 1990; 51: 229–234.

    PubMed  CAS  Google Scholar 

  41. Stoorvogel W, Strous GJ, Geuze HJ et al. Late endosomes derive from early endosomes by maturation. Cell 1991; 65: 417–427.

    PubMed  CAS  Google Scholar 

  42. Murphy RF. Maturation models for endosome and lysosome biogenesis. Trends Cell Biol 1991; 1: 77–82.

    PubMed  CAS  Google Scholar 

  43. Futter CE, Pearse A, Hewlett LJ et al. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 1996; 132: 1011–1023.

    PubMed  CAS  Google Scholar 

  44. Hopkins CR, Gibson A, Shipman M, Miller K. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 1990; 346: 335–339.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  46. Futter CES, Felder S, Schlessinger J et al. Annexin 1 is phosphorylated in the multivesicular body during the processing of the epidermal growth factor. J Cell Biol 1993; 120: 77–83.

    PubMed  CAS  Google Scholar 

  47. Schlossman DM, Schmid SL, Brae11 WA et al. An enzyme that removes clathrin coats: purification of an uncoating ATPase. J Cell Biol 1984; 99: 723–733.

    PubMed  CAS  Google Scholar 

  48. Davis JQ, Dansereau D, Johnstone RM et al. Selective externalization of an ATP-binding protein structurally related to the clathrin-uncoating ATPase/heat shock protein in vesicles containing terminal transferrin receptors during reticulocyte maturation. J Biol Chem 1986; 261: 15368–15371.

    PubMed  CAS  Google Scholar 

  49. Kurten RC, Cadena DL, Gill GN. Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 1996; 272: 1008–1010.

    PubMed  CAS  Google Scholar 

  50. Geuze HJ, Stoorvogel W, Strous GJ et al. Sorting of mannose-6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. 107 1988; 2491–2501.

    CAS  Google Scholar 

  51. Klumperman J, Hille A, Veenendaal T et al. Differences in the endosomal distributions of the two mannose-6-phosphate receptors. J Cell Biol 1993; 121: 997–1010.

    PubMed  CAS  Google Scholar 

  52. Pfeffer SR, Rothman JE. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Ann Rev Biochem 1987; 56: 829–852.

    PubMed  CAS  Google Scholar 

  53. Matter K, Mellman I. Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr Opin Cell Biol 1994; 6: 545–554.

    PubMed  CAS  Google Scholar 

  54. Simons K. Biogenesis of epithelial cell surface polarity. Harvey Lect. 1995; 89: 125–146.

    Google Scholar 

  55. Yoshimori T, Keller P, Roth MG et al. Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells. J Cell Biol 1996; 133: 247–256.

    PubMed  CAS  Google Scholar 

  56. Gerdes HH, Rosa P, Phillips E et al. The primary structure of hman secretogranin II: a widespread tyrosine-sulfated secretory protein that exhibits low pH and a calcium induced aggregation. J Biol Chem 1989; 264: 12009–12015.

    PubMed  CAS  Google Scholar 

  57. Wagner DD, Saffaripour S, Bonfanti R et al. Induction of specific storage organelles by von Willebrand factor propolypeptide. Cell 1991; 64: 403–413.

    PubMed  CAS  Google Scholar 

  58. Chanat E, Huttner WB. Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 1991; 115: 1505–1519.

    PubMed  CAS  Google Scholar 

  59. Bauerfeind R, Huttner WB. Biogenesis of constitutive secretory vesicles, secretory granules and synaptic vesicles. Curr Opin Cell Biol 1993; 5: 628–635.

    PubMed  CAS  Google Scholar 

  60. Kuliawat R, Aryan P. Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic 13-cells. J Cell Biol 1994; 126: 77–86.

    PubMed  CAS  Google Scholar 

  61. Tapper H. The secretion of preformed granules by macrophages and neutrophils. J Leukoc Biol 1996; 59: 613–622.

    PubMed  CAS  Google Scholar 

  62. Voorhout WF, Weaver TE, Haagsman HP et al. Biosynthetic routing of pulmonary surfactant proteins in alveolar type II cells. Microsc Res Tech 1993; 26: 366–373.

    PubMed  CAS  Google Scholar 

  63. Baron R. Molecular mechanisms of bone resorption. An update. Acta Orthopaedica Scandinavica Suppl. 1995; 266: 66–70.

    CAS  Google Scholar 

  64. Podack ER, Young JDE, Cohn ZA. Isolation and characterization of perforin 1 from cytolytic T cell granules. Proc Natl Acad Sci USA 1985; 82: 8629–8633.

    PubMed  CAS  Google Scholar 

  65. Schmid SL, Rothman JE. Enzymatic dissociation of clathrin cages in a two-stage process. J Biol Chem 1985; 260: 10044–10049.

    PubMed  CAS  Google Scholar 

  66. Bu G, Schwartz AL. Receptor-mediated endocytosis. The liver: Biology and pathology. Third ed. New-York: Raven Press, Ltd., 1994; 259–274.

    Google Scholar 

  67. Li CY, Watkins JA, Glass J. The +H-ATPase from reticulocyte endosomes reconstituted into liposomes acts as an iron transporter. J Biol Chem 1994; 269: 10242–10246.

    PubMed  CAS  Google Scholar 

  68. Dautry-Varsat A, Ciechanover A, Lodish HF. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci USA 1983; 80: 2258–2262.

    PubMed  CAS  Google Scholar 

  69. van Bockxmeer FM, Morgan EH. Transferrin receptors during rabbit reticulocyte maturation. Bioch Biophys Acta 1979; 584: 76–83.

    Google Scholar 

  70. Johnstone RM. The transferrin receptor. In: Parker PAaJC, ed. Hematology: red blood cell membranes. New York: M. Dekker, 1989; 11: 325–365.

    Google Scholar 

  71. Johnson LS, Dunn KW, Pytowski B et al. Endosome acidification and receptor trafficking: bafilomycin Al slows receptor externalization by a mechanism involving the receptor’s internalization motif. Mol Biol Cell 1993; 4: 1251–1266.

    PubMed  CAS  Google Scholar 

  72. Aniento F, Parton RG, Gruenberg J. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 1996; 133: 29–41.

    PubMed  CAS  Google Scholar 

  73. Simons K, Wandinger-Ness A. Polarized sorting in epithelia. Cell 1990; 62: 207–210.

    PubMed  CAS  Google Scholar 

  74. Sandhoff K, Klein A. Intracellular trafficking of glycosphingolipids: role of sphingolipid activator proteins in the topology of endocytosis and lysosomal digestion. FEBS Lett 1994; 346: 103–107.

    PubMed  CAS  Google Scholar 

  75. Felder S, Miller K, Moehren G et al. Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 1990; 61: 623–634.

    PubMed  CAS  Google Scholar 

  76. Shih YJ, Baynes RD, Hudson BG et al. Serum transferrin is a truncated form of the tissue receptor. J Biol Chem 1990; 265: 19077–19081.

    PubMed  CAS  Google Scholar 

  77. Cresswell P. Assembly, transport, and function of MHC class II molecules. Ann Rev Immunol 1994; 12: 259–293.

    CAS  Google Scholar 

  78. Wolf PR, Ploegh HL. How MHC class II molecules acquire peptide cargo: Biosynthesis and trafficking through the endocytic pathway. Ann Rev Cell Dev Biol 1995; 11: 267–306.

    CAS  Google Scholar 

  79. Marks MS, Blum JS, Cresswell P. Invariant chain trimers are sequestered in the RER in the absence of association with HLA class II antigens. J Cell Biol 1990; 111: 839–855.

    PubMed  CAS  Google Scholar 

  80. Cresswell P. Invariant chain structure and MHC class II function. Cell 1996; 84: 505–507.

    PubMed  CAS  Google Scholar 

  81. Neefjes JJ, Stollorz V, Peters PJ et al. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 1990; 61: 171–183.

    PubMed  CAS  Google Scholar 

  82. Peters PJ, Neefjes JJ, Oorschot V et al. Segregation of MHC class-II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 1991; 349: 669–676.

    PubMed  CAS  Google Scholar 

  83. Morton PA, Zacheis ML, Giacoletto KS et al. Delivery of nascent MHC class II-invariant chain by cystein proteases precedes peptide binding in B-lymphoblastoid cells. J Immunol 1995; 154: 137–150.

    PubMed  CAS  Google Scholar 

  84. Riese RJ, Wolf PR, Brömme D et al. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 1996; 4: 357–366.

    PubMed  CAS  Google Scholar 

  85. Sloan VS, Camerson P, Porter G et al. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 1995; 375: 802–806.

    PubMed  CAS  Google Scholar 

  86. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II a/13 dimers and facilitates peptide loading. Cell 1995; 82: 155–165.

    PubMed  CAS  Google Scholar 

  87. Germain RN. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 1994; 76: 287–299.

    PubMed  CAS  Google Scholar 

  88. Kleijmeer M, Oorschot V, Geuze HJ. Human Langerhans cells display a lysosomal compartment enriched in MHC class II. J Invest Dermatol 1994; 103: 516–523.

    PubMed  CAS  Google Scholar 

  89. Nijman HW, Kleijmeer MJ, Ossevort MA et al. Antigen capture and MHC class II compartments in freshly isolated and cultured blood dendritic cells. J Exp Med 1995; 182: 163–174.

    PubMed  CAS  Google Scholar 

  90. Peters P, Raposo G, Neefjes JJ et al. MHC class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J Exp Med 1995; 325–334.

    Google Scholar 

  91. Glickman JN, Morton PA, Slot JW et al. The biogenesis of MHC class II compartment in human I-cell disease B lymphoblasts. J Cell Biol 1996; 132: 769–785.

    PubMed  CAS  Google Scholar 

  92. Qiu Y, Xu X, Wandinger-Ness A et al. Separation of subcellular compartments containing distinct functional forms of MHC class II. J Cell Biol 1994; 125: 595–605.

    PubMed  CAS  Google Scholar 

  93. Rudensky AY, Maric M, Eastman S et al. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity 1994; 1: 585–594.

    PubMed  CAS  Google Scholar 

  94. Tulp A, Verwoerd D, Dobberstein B et al. Isolation and characterization of the intracellular MHC class II compartment. Nature 1994; 369: 120–126.

    PubMed  CAS  Google Scholar 

  95. West MA, Lucocq JM, Watts C. Antigen processing and class II MHC peptide-loading compartments in human B-Iymphoblastoid cells. Nature 1994; 369: 147–151.

    PubMed  CAS  Google Scholar 

  96. Sanderson F, Kleijmeer MJ, Kelly A et al. Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 1994; 266: 1566–1569.

    PubMed  CAS  Google Scholar 

  97. Amigorena S, Drake JR, Webster P et al. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 1994; 369: 113–120.

    PubMed  CAS  Google Scholar 

  98. Castellino F, Germain RN. Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 1995; 2: 73–88.

    PubMed  CAS  Google Scholar 

  99. Lippincott-Schwartz J, Fambrough DM. Cycling of the integral membrane glycoprotein, LEP 100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell 1987; 49: 669–677.

    PubMed  CAS  Google Scholar 

  100. Harter C, Mellman I. transport of the lysosomal membrane glycopro-tein lgp 120 (lgp-A) to lysosomes does not require appearance on the plasma membrane. J Cell Biol 1992; 117: 311–325.

    PubMed  CAS  Google Scholar 

  101. Emerson SG, Cone RE. Turnover and shedding of la antigens by murine spleen cells in culture. J Immunol 1979; 122: 892–899.

    PubMed  CAS  Google Scholar 

  102. Emerson SG, Cone RE. I-Kk and H-2Kk antigens are shed as supramolecular particles in association with membrane lipids. J Immunol 1981; 127: 482–486.

    PubMed  CAS  Google Scholar 

  103. Sachs DH, Kiszkiss P, Kim KJ. Release of la antigens by a cultured B cell line. J Immunol 1980; 124: 2130–2136.

    PubMed  CAS  Google Scholar 

  104. Callahan GN, Ferrone S, Poulik MD et al. Characterization of la antigens in mouse serum. J Immunol 1976; 117: 1351–1355.

    PubMed  CAS  Google Scholar 

  105. Gray D, Kosco M, Stockinger B. Novel pathways of antigen presentation for the maintenance of memory. Int Immunol 1991; 3: 141–148.

    PubMed  CAS  Google Scholar 

  106. Meeusen E. The induction of cytotoxic T cell responses with H-2 antigens shed from viable lymphocytes. Immunol 1987; 61: 321–326.

    CAS  Google Scholar 

  107. Masson D, Tschopp J. Isolation of a lytic, pore-forming protein (perforin) from cytolytic T lymphocytes. J Biol Chem 1985; 260: 9069–9072.

    PubMed  CAS  Google Scholar 

  108. Baetz K, Isaaz S, Griffiths GM. Loss of cytotoxic T lymphocyte function in Chediak-Higashi syndrome arises from a secretory defect that prevents lytic granule exocytosis. J Immunol 1995; 154: 6122–6131.

    PubMed  CAS  Google Scholar 

  109. Young JD, Liu CC, Persechini PM, Cohn ZA. Perforin-dependent and–independent pathways of cytotoxicity mediated by lymphocytes. Immunological Rev 1988; 103: 161–202.

    CAS  Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Raposo, G., Vidal, M., Geuze, H. (1997). Secretory Lysosomes and the Production of Exosomes. In: Unusual Secretory Pathways: From Bacteria to Man. Molecular Biology Intelligence Unit. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-22581-3_6

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-22581-3_6

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-22583-7

  • Online ISBN: 978-3-662-22581-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Navigation