Skip to main content
SpringerLink
Log in
Book cover

Molecular Biology of Membrane Transport Disorders pp 303–319Cite as

Receptor-Mediated Endocytosis

  • Chapter

Abstract

In order to sustain normal metabolic processes, the cell must recruit from its external environment an array of ions, molecules, and macromolecules. Small molecules, such as ions, water, and monosaccharides, can gain entry into the cytosol of the cell through water-filled channels. However, molecules larger than approximately 1000 Da cannot pass through these channels. Therefore, if diffusion through plasma membrane pores or channels were the only method of entry into the cell cytoplasm, larger molecules such as polypeptides, polysaccharides, and other nutrients could not be utilized by the cell for normal metabolic processes. In addition, these larger molecules are often present in the extracellular environment of the cell at much lower concentrations than ions or monosaccharides. Therefore, in order to overcome problems associated with internalizing large and scarce molecules, the cell has developed the process of receptor-mediated endocytosis. The extracellular macromolecules bind to specific, high-affinity receptors on the cell surface, thereby trapping them and concentrating these macromolecules at the plasma membrane.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Goldstein, J. L., Brown, M. S., Anderson, R. G. W., Russell, D. W., and Schneider, W. J. Receptor-mediated endocytosis: Concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1:1–39.

    Google Scholar 

  2. Levitzki, A. (1985). Receptors. In Endocytosis (I. Pastan and M. C. Willingham, eds.), Plenum Press, New York, pp. 45–68.

    Google Scholar 

  3. Anderson, R. G. W. (1991). Molecular motors that shape endocytic membrane. In Intracellular Trafficking of Proteins (C. J. Steer and J. A. Hanover, eds.), Cambridge University Press, London, pp. 13–47.

    Google Scholar 

  4. Pearse, B. M. F., and Robinson, M. S. (1990). Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6:151–171.

    PubMed  CAS  Google Scholar 

  5. Hansen, S. H., Sandvig, K., and Van Deurs, B. (1993). Clathrin and HA2 adaptors: Effects of potassium depletion, hypertonic medium, and cytosol acidification. J. Cell Biol. 121:61–72.

    PubMed  CAS  Google Scholar 

  6. Mahaffey, D. T., Moore, M. S., Brodsky, F. M., and Anderson, R. G. W. (1989). Coat proteins isolated from clathrin coated vesicles can assemble into coated pits. J. Cell Biol. 108:1615–1624.

    PubMed  CAS  Google Scholar 

  7. Moore, M. S., Mahaffey, D. T., Brodsky, F. M., and Anderson, R. G. W. (1989). Assembly of clathrin-coated pits onto purified plasma membranes. Science 263:558–563.

    Google Scholar 

  8. Chang, M.-R, Mallet, W. G., Mostov, K. E., and Brodsky, F. M. (1993). Adaptor self-aggregation, adaptor-receptor recognition and binding of alpha-adaptin subunits to the plasma membrane contribute to recruitment of adaptor (AP2) components to clathrin-coated pits. EMBO J. 12:2169–2180.

    PubMed  CAS  Google Scholar 

  9. Peeler, J. S., Donzell, W. C., and Anderson, R. G. W. (1993). The appendage domain of the AP-2 subunit is not required for assembly or invagination of clathrin-coated pits. J. Cell Biol. 120:47–54.

    PubMed  CAS  Google Scholar 

  10. Heuser, J. E., and Anderson, R. G. W. (1988). Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108:389–400.

    Google Scholar 

  11. Sorkin, A., and Carpenter, G. (1993). Interaction of activated EGF receptors with coated pit adaptins. Science 261:612–615.

    PubMed  CAS  Google Scholar 

  12. Collawn, J. F., Stangel, M., Kuhn, L. A., Esekogwu, V., Jing, S., Trowbridge, I. S., and Tainer, J. A. (1990). Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 63:1061–1072.

    PubMed  CAS  Google Scholar 

  13. Trowbridge, I. S. (1991). Endocytosis and signals for internalisation. Curr. Opin. Cell Biol. 3:634–641.

    PubMed  CAS  Google Scholar 

  14. Watts, C., and Marsh, M. (1992). Endocytosis: What goes in and how? J. Cell Sci. 103:1–8.

    PubMed  Google Scholar 

  15. Vallee, R. B. (1992). Dynamin: Motor protein or regulatory GTPase. J. Muscle Res. Cell. Motil. 13:493–496.

    PubMed  CAS  Google Scholar 

  16. Lin, H. C., Moore, M. S., Sanan, D. A., and Anderson, R. G. W. (1991). Reconstitution of coated pit budding from plasma membranes. J. Cell Biol. 114:881–891.

    PubMed  CAS  Google Scholar 

  17. Carter, L. L., Redelmeier, T. E., Woollenweber, L. A., and Schmid, S. L. (1993). Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis. J. Cell Biol. 120:37–45.

    PubMed  CAS  Google Scholar 

  18. Blum, J. S., Diaz, R., Mayorga, L. S., and Stahl, P. D. (1993). Re-constitution of endosomal transport and proteolysis. In Subcellular Biochemistry. Endocytic Components: Identification and Characterization (J. J. M. Bergeron and J. R. Harris, eds.), Plenum Press, New York, pp. 69–93.

    Google Scholar 

  19. Brown, M. S., Anderson, R. G. W., and Goldstein, J. L. (1983). Recycling receptors: The round-trip itinerary of migrant membrane proteins. Cell 32:663–667.

    PubMed  CAS  Google Scholar 

  20. Maxfield, F. R. (1985). Acidification of endocytic vesicles and lysosomes. In Endocytosis (I. Pastan and M. C. Willingham, eds.), Plenum Press, New York, pp. 235–257.

    Google Scholar 

  21. Salzman, N. H., and Maxfield, F. R. (1993). Quantitative fluorescence techniques for the characterization of endocytosis in intact cells. In Subcellular Biochemistry. Endocytic Components: Identification and Characterization (J. J. M. Bergeron and J. R. Harris, eds.), Plenum Press, New York, pp. 95–123.

    Google Scholar 

  22. Schmid, S., Fuchs, R., Kielian, M., Helenius, A., and Mellman, I. (1989). Acidification of endosome subpopulations in wild-type Chinese hamster ovary cells and temperature-sensitive acidification-defective mutants. J. Cell Biol. 108:1291–1300.

    PubMed  CAS  Google Scholar 

  23. Forgac, M. (1992). Structure, function and regulation of the coated vesicle V-ATPase. J. Exp. Biol. 172:155–169.

    PubMed  CAS  Google Scholar 

  24. Fuchs, R., Male, P., and Mellman, I. (1989). Acidification and ion permeabilities of highly purified rat liver endosomes. J. Biol. Chem. 264:221–230.

    Google Scholar 

  25. Fuchs, R., Schmid, S., and Mellman, I. (1989). A possible role for Na+ K+-ATPase in regulating ATP-dependent endosome acidification. Proc. Natl. Acad. Sci. USA 86:539–543.

    PubMed  CAS  Google Scholar 

  26. Kane, P. M., Kuehn, M. C., Howald-Stevenson, I., and Stevens, T. H. (1992). Assembly and targeting of peripheral and integral membrane subunits of the yeast vacuolar (H(+)-ATPase. J. Biol. Chem. 267:447–454.

    PubMed  CAS  Google Scholar 

  27. Ho, M. N., Hill, K. J., Lindorfer, M. A., and Stevens, T. H. (1993). Isolation of vacuolar membrane H(+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H(+)-ATPase. J. Biol. Chem. 268:221–227.

    PubMed  CAS  Google Scholar 

  28. Hirata, R., Umemoto, N., Ho, M. N., Ohya, Y, Stevens, T. H., and Anraku, Y (1993). VMA12 is essential for assembly of the vacuolar H(+)-ATPase subunits onto the vacuolar membrane in Saccha-romyces cerevisiae. J. Biol. Chem. 268:961–967.

    PubMed  CAS  Google Scholar 

  29. Mellman, I. (1992). The importance of being acid: The role of acidification in intracellular membrane traffic. J. Exp. Biol. 172:39–45.

    PubMed  CAS  Google Scholar 

  30. Geffen, I., and Spiess, M. (1992). Asialoglycoprotein receptor. Int. Rev. Cytol. 137B:181–219.

    PubMed  CAS  Google Scholar 

  31. Hamel, F. G., Posner, B. I., Bergeron, J. J. M., Frank, B. H., and Duckworth, W. C. (1988). Isolation of insulin degradation products from endosomes derived from intact rat liver. J. Biol. Chem. 263:6703–6708.

    PubMed  CAS  Google Scholar 

  32. Doherty, J.-J., II, Kay, D. G., Lai, W. H., Posner, B. I., and Bergeron, J. J. M. (1990). Selective degradation of insulin within rat liver endosomes. J. Cell Biol. 110:35–42.

    PubMed  CAS  Google Scholar 

  33. Knutson, V. P. (1992). Ligand-independent internalization and recycling of the insulin receptor. Effects of chronic treatment of 3T3-C2 fibroblasts with insulin and dexamethasone. J. Biol. Chem. 267:931–937.

    PubMed  CAS  Google Scholar 

  34. Diment, S., and Stahl, P. (1985). Macrophage endosomes contain proteases which degrade endocytosed protein ligands. J. Biol. Chem. 260:15311–15317.

    PubMed  CAS  Google Scholar 

  35. Rodman, J. S., Levy, M. A., Diment, S., and Stahl, P. D. Immunolo-calization of endosomal cathepsin D in rabbit alveolar macrophages. J. Leuk.Biol. 48:116–122.

    Google Scholar 

  36. Blum, J. S., Fiani, M. L., and Stahl, P. D. (1989). Characterization of neutral and acidic proteases in endosomal vesicles. J. Cell Biol. 109:188a (Abstract).

    Google Scholar 

  37. Casciola-Rosen, L. A., Renfrew, C. A., and Hubbard, A. L. (1992). Lumenal labeling of rat hepatocyte endocytic compartments: Distribution of several acid hydrolases and membrane receptors. J. Biol. Chem. 267:11856–11864.

    PubMed  CAS  Google Scholar 

  38. Rodman, J. S., Levy, M. A., Diment, S., and Stahl, P. D. (1990). Im-munolocalization of endosomal cathepsin D in rabbit alveolar macrophages. J. Leuk. Biol. 48:116–122.

    CAS  Google Scholar 

  39. Roederer, M., Bowser, R., and Murphy, R. F. (1987). Kinetics and temperature dependence of exposure of endocytosed material to proteolytic enzymes and low pH; evidence for a maturation model for the formation of lysosomes. J. Cell. Physiol. 131:200–209.

    PubMed  CAS  Google Scholar 

  40. Blum, J. S., Fiani, M. L., and Stahl, P. D. (1992). Proteolytic cleavage of ricin A chain in endosomal vesicles. Evidence for the action of endosomal proteases at both neutral and acidic pH. J. Biol. Chem. 266:22091–22095.

    Google Scholar 

  41. Renfrew, C. A., and Hubbard, A. L. (1991). Sequential processing of epidermal growth factor in early and late endosomes of rat liver. J. Biol. Chem. 266:4348–4356.

    PubMed  CAS  Google Scholar 

  42. Knutson, V. P. (1991). Proteolytic processing of the insulin receptor β subunit is associated with insulin-induced receptor down-regulation. J. Biol. Chem. 266:15656–15662.

    PubMed  CAS  Google Scholar 

  43. Zupan, A. A., and Johnson, E. M., Jr. (1991). Evidence for endocyto-sis-dependent proteolysis in the generation of soluble truncated nerve growth factor receptors by A875 human melanoma cells. J. Biol. Chem. 266:15384–15390.

    PubMed  CAS  Google Scholar 

  44. Wicker, G., Prill, V., Brooks, D., Gibson, G., Hopwood, J., Von Figura, K., and Peters, C. (1992). Mucopolysaccharidosis VI (Maroteaux-Iamy syndrome). An intermediate clinical phenotype caused by substitution of valine for glycine at position 137 of aryl-sulfatase B. J. Biol. Chem. 266:21386–21391.

    Google Scholar 

  45. Hobbs, H. H., Brown, M. A., and Goldstein, J. L. (1992). Molecular genetics of the LDL receptor gene in familial hypercholesterolemia. Hum. Mutat. 1:445–466.

    PubMed  CAS  Google Scholar 

  46. Grossman, M., and Wilson, J. M. (1992). Frontiers in gene therapy: LDL receptor replacement for hypercholesterolemia. J. Lab. Clin. Med. 119:457–460.

    PubMed  CAS  Google Scholar 

  47. Tybjaerg-Hansen, A., and Humphries, S. E. (1992). Familial defective apolipoprotein B-100: A single mutation that causes hypercholesterolemia and premature coronary artery disease. Atherosclerosis 96:91–107.

    PubMed  CAS  Google Scholar 

  48. Morgan, E. H., and Baker, E. (1988). Role of transferrin receptors and endocytosis in iron uptake by hepatic and erythroid cells. Ann N.Y.Acad. Sci. 526:65–82.

    PubMed  CAS  Google Scholar 

  49. Bonkovsky, H. L. (1991). Iron and the liver. Am. J. Med. Sci. 301:32–43.

    PubMed  CAS  Google Scholar 

  50. Seligman, P. A., Klausner, R. D., and Huebers, H. A. (1987). Molecular mechanisms of iron metabolism. In The Molecular Basis of Blood Diseases (G. Stamatoyannopoulos, A. W. Nienhuis, P. Leder, et al., eds.), Saunders, Philadelphia, pp. 219–244.

    Google Scholar 

  51. Iacopetta, B. J., and Morgan, E. H. (1983). The kinetics of transferrin endocytosis and iron uptake from transferrin in rabbit reticulocytes. J. Biol. Chem. 258:9108–9115.

    PubMed  CAS  Google Scholar 

  52. Hentze, M. W., Rouault, T. A., Harford, J. B., and Klausner, R. D. (1989). Oxidation-reduction and the molecular mechanism of a regulatory RNA-protein interaction. Science 244:357–359.

    PubMed  CAS  Google Scholar 

  53. Rouault, T. A., Hentze, M. W., Haile, D. J., Klausner, R. D., and Harford, J. B. (1989). The RNA-binding protein that interacts with the iron-responsive elements found in transferrin receptor and ferritin mRNA’s: Isolation and partial characterization of the human protein. Abstracts of IXth International Conference on Proteins of Iron Transport and Storage, Brisbane, p. 19.

    Google Scholar 

  54. Sciot, R., Paterson, A. C., Van den Oord, J. J., and Desmet, V. J. (1987). Lack of hepatic transferrin receptor expression in hemochromatosis. Hepatology 7:831–837.

    PubMed  CAS  Google Scholar 

  55. Abe, Y., Muta, K., Mishimura, J., and Nawata, H. (1992). Regulation of transferrin receptors by iron in human erythroblasts. Am. J. Hematol. 40:270–275.

    PubMed  CAS  Google Scholar 

  56. Thorstensen, K., and Romslo, I. (1993). The transferrin receptor: Its diagnostic value and its potential as therapeutic target. Scand. J. Clin. Lab. Invest. 215:113–120.

    CAS  Google Scholar 

  57. Raub, T. J., and Newton, C. R. (1991). Recycling kinetics and transcytosis of transferrin in primary cultures of bovine brain microvessel endothelial cells. J. Cell. Physiol. 149:141–151.

    PubMed  CAS  Google Scholar 

  58. Drickamer, K., and Taylor, M. E. (1993). Biology of animal lectins. Annu. Rev. Cell Biol. 9:237–264.

    PubMed  CAS  Google Scholar 

  59. Geffen, I., Wessels, H. P., Roth, J., Shia, M. A., and Spiess, M. (1989). Endocytosis and recycling of subunit H1 of the asialoglyco-protein receptor is independent of oligomerization with H2. EMBO J. 8:2855–2862.

    PubMed  CAS  Google Scholar 

  60. Steer, C. J., Weiss, P., Huber, B. E., Wirth, P. J., Thorgeirsson, S. S., and Ashwell, G. (1987). Ligand-induced modulation of the hepatic receptor for asialoglycoproteins in the human hepatoblastoma cell line, Hep G2. J. Biol. Chem. 262:17524–17529.

    PubMed  CAS  Google Scholar 

  61. Breitfeld, P. P., Simmons, C. F., Strous, G. J. A. M., Geuze, H. J., and Schwartz, A. L. (1985). Cell biology of the asialoglycoprotein receptor system: A model of receptor-mediated endocytosis. Int. Rev. Cytol. 97:47–95.

    PubMed  CAS  Google Scholar 

  62. Lee, Y. C., Townsend, R. R., Hardy, M. R., Lonngren, J., Arnarp, J., Haraldsson, M. and Lonn, H. (1983). Binding of synthetic oligosaccharides to the hepatic Gal/GalNAc lectin. Dependence on fine structural features. J. Biol. Chem. 258:199–202.

    PubMed  CAS  Google Scholar 

  63. Weigel, P. H. (1993). Endocytosis and function of the hepatic asialoglycoprotein receptor. Subcell. Biochem. 19:125–161.

    PubMed  CAS  Google Scholar 

  64. Windier, E., Greeve, J., Levkau, B., Kolb-Bachofen, V., Daerr, W., and Greten, H. (1991). The human asialoglycoprotein receptor is a possible binding site for low-density lipoproteins and chylomicron remnants. Biochem. J. 276:79–87.

    Google Scholar 

  65. Zannis, V. I., McPherson, J., Goldberger, G., Karathanasis, S. K., and Breslow, J. L. (1984). Synthesis, intracellular processing, and signal peptide of human apolipoprotein E. J. Biol. Chem. 259:5495–5499.

    PubMed  CAS  Google Scholar 

  66. Brown, W. R., and Kloppel, T. M. (1989). The liver and IgA: Immunological, cell biological and clinical implications. Hepatology 9:763–784.

    PubMed  CAS  Google Scholar 

  67. Daniels, C. K., Schmucker, D. L., and Jones, A. L. (1989). Hepatic asialoglycoprotein receptor-mediated binding of human polymeric immunoglobulin A. Hepatology 9:229–234.

    PubMed  CAS  Google Scholar 

  68. Mestecky, J., Moldoveanu, Z., Tomana, M., Epps, J. M., Thorpe, S. R., Phillips, J. O., and Kulhavy, R. (1989). The role of the liver in catabolism of mouse and human IgA. Immunol. Invest. 18:313–324.

    PubMed  CAS  Google Scholar 

  69. Aminoff, D. (1988). The role of sialoglycoconjugates in the aging and sequestration of red blood cells from circulation. Blood Cells 14:229–247.

    PubMed  CAS  Google Scholar 

  70. Schlepper-Schafer, J., and Kolb-Bachofen, V. (1988). Red cell aging results in a change of cell surface carbohydrate epitopes allowing for recognition by galactose-specific receptors of rat liver macrophages. Blood Cells 14:259–269.

    PubMed  CAS  Google Scholar 

  71. Pontow, S. E., Kery, V., and Stahl, P. D. (1992). Mannose receptor. Int. Rev. Cytol. 137B:221–244.

    PubMed  CAS  Google Scholar 

  72. Shepherd, V. L., and Hoidal, J. R. (1990). Clearance of neutrophil-derived myeloperoxidase by the macrophage mannose receptor. Am. J. Respir. Cell. Mol. Biol. 2:335–340.

    PubMed  CAS  Google Scholar 

  73. Otter, M., Kuiper, J., van Berkel, T. J., and Rijken, D. C. (1992). Mechanisms of tissue-type plasminogen activator (tPA) clearance by the liver. Ann. N.Y.Acad. Sci. 667:431–442.

    PubMed  CAS  Google Scholar 

  74. Rijnboutt, S., Kal, A. J., Geuze, H. J., Aerts, A., and Strous, G. J. (1991). Mannose 6-phosphate-independent targeting of cathepsin D to lysosomes in HepG2 cells. J. Biol. Chem. 266:23586–23592.

    PubMed  CAS  Google Scholar 

  75. Ezekowitz, R. A., Williams, D. J., Koziel, H., (1991). Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351:155–158.

    PubMed  CAS  Google Scholar 

  76. Kruskal, B. A., Sastry, K., Warner, A. B., Mathieu, C. E., and Ezekowitz, R. A. (1992). Phagocytic chimeric receptors require both transmembrane and cytoplasmic domains from the mannose receptor. J. Exp. Med. 176:1673–1680.

    PubMed  CAS  Google Scholar 

  77. Harris, M., Super, M., Rits, M., Chang, G., and Ezekowitz, R. A. (1992). Characterization of the murine macrophage mannose receptor: Demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription. Blood 80:2363–2373.

    PubMed  CAS  Google Scholar 

  78. Koziel, H., Kruskal, B. A., Ezekowitz, R. A., and Rose, R. M. (1993). HIV impairs alveolar macrophage mannose receptor function against Pneumocystis carinii. Chest 103:111S–112S.

    PubMed  CAS  Google Scholar 

  79. Borth, W. (1992). α2-Macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J. 6:3345–3353.

    PubMed  CAS  Google Scholar 

  80. Araujojorge, T. C., Lage, M. J. F., Rivera, M. T., Carlier, Z., and Van Leuven, F. (1992). Trypanosoma cruzi-enhanced alpha-macroglobu-lin levels correlate with the resistance of BALB/cj mice to acute infection. Parasitol. Res. 78:215–221.

    CAS  Google Scholar 

  81. Miyagawa, S., Nishino, N., Kamata, R., Okamura, R., and Maeda, H. (1991). Effects of proteinase inhibitors on growth of Serratia marcescens and Pseudomonas aeruginosa. Microb. Pathol. 11:137–141.

    CAS  Google Scholar 

  82. Yamashiro, D. J., Borden, L. A., and Maxfield, F. R. (1989). Kinetics of α2-macroglobulin endocytosis and degradation in mutant and wild-type Chinese hamster ovary cells. J. Cell. Physiol. 139:377–382.

    PubMed  CAS  Google Scholar 

  83. Maeda, H., Molla, A., Oda, T., and Katsuki, T. (1987). Internalization of serratial protease into cells as an enzyme-inhibitor complex with α2-macroglobulin and regeneration of protease activity and cytotoxicity. J. Biol. Chem. 262:10946–10950.

    PubMed  CAS  Google Scholar 

  84. Hofer, F., Gruenberger, M., Kowalski, H., Machat, H., Huettinger, M., Kuechler, E., and Blass, D. (1994). Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc. Natl. Acad. Sci. USA 91:1839–1842.

    PubMed  CAS  Google Scholar 

  85. Gonias, S. J. (1992). α2-Macroglobulin: A protein at the interface of fibrinolysis and cellular growth regulation. Exp. Hematol. 20:302–311.

    PubMed  CAS  Google Scholar 

  86. Koo, P. H., and Stach, R. W. (1989). Interaction of nerve growth factor with murine α-macroglobulin. J. Neurosci. Res. 22:247–261.

    PubMed  CAS  Google Scholar 

  87. Misra, U. K., Chu, C. T., Gawdi, G., and Pizzo, S. V. (1994). Evidence for a second alpha 2-macroglobulin receptor. J. Biol. Chem. 269:12541–12547.

    PubMed  CAS  Google Scholar 

  88. Kounnas, M. Z., Morris, R. E., Thompson, M. R., FitzGerald, D. J., Strickland, D. K., and Saelinger, C. B. (1992). The α2-macroglobu-lin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A. J. Biol. Chem. 267:12420–12423.

    PubMed  CAS  Google Scholar 

  89. Nykjoer, A., Peterson, M. C., Moller, M., Jensen, P. H., Moestrup, S. K., Holtet, T. L., Etyerodt, M., Thogersen, J. C., Munch, M., Andreasen, P. A., and Gliemann, J. (1992). Purified α2-macroglobulin receptor/LDL receptor-related protein binds urokinase plasminogen activator inhibitor type 2 complex. Evidence that the α2-macroglob-ulin receptor mediates cellular degradation of urokinase receptor-bound complexes. J. Biol. Chem. 267:14543–14546.

    Google Scholar 

  90. Andreasen, P. A., Sottrup-Jensen, L., Kjoller, L., Nykjaer, A., Moestrup, S. K., Peterson, C. M, and Gliemann, J. (1994). Receptor-mediated endocytosis of plasminogen activators and activator/ inhibitor complexes. FEBS Lett. 338:239–245.

    PubMed  CAS  Google Scholar 

  91. Cooper, A. D. (1992). Hepatic clearance of plasma chylomicron remnants. Semin. Liver Dis. 12:386–396.

    PubMed  CAS  Google Scholar 

  92. Strickland, K. D., Ashcom, J. D., and Williams S. (1990). Sequence identity between the α2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J. Biol. Chem. 265:17401–17404.

    PubMed  CAS  Google Scholar 

  93. Hussain, M. M., Maxfield, F. R., and Mas-Oliva, J. (1991). Clearance of chylomicron remnants by the low density lipoprotein receptor-related protein/α2-macroglobulin receptor. J. Biol. Chem. 266:13936–13940.

    PubMed  CAS  Google Scholar 

  94. Luoma, J., Hiltunen, T., Sarkioja, T., Moestrup, S. K., Gliemann, J., Kodama, T., Nikkari, T., and Yla-Herttuala, S. (1994). Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein and scavenger receptor in human atherosclerotic lesions. J. Clin. Invest. 93:2014–2021.

    PubMed  CAS  Google Scholar 

  95. Rasmussen, L. K., Sorensen, E. S., Petersen, T. E., Gliemann, J., and Jensen, P. H. (1994). Identification of glutamine and lysine residues in Alzheimer amyloid beta A4 peptide responsible for transglutaminase-catalyzed homopolymerization and cross-linking to alpha 2 M receptor. FEBS Lett. 338:161–166.

    PubMed  CAS  Google Scholar 

  96. Barber, L. D., and Parham, P. (1993). Peptide binding to major histocompatibility complex molecules. Anna. Ref. Cell Biol. 9:163–206.

    CAS  Google Scholar 

  97. Chicz, R. M., Urban, R. G., Lane, W. S., Gorga, J. C., and Stern, L. J. (1992). Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 358:764–768.

    PubMed  CAS  Google Scholar 

  98. Nelson, C. A., Roof, R. W., McCourt, D. W., and Unanue, E. R. (1992). Identification of the naturally processed form of hen egg white lysozyme bound to the murine histocompatibility complex class II molecule I-Ak. Proc. Natl. Acad. Sci. USA 89:7380–7383.

    PubMed  CAS  Google Scholar 

  99. Brodsky, F. M. (1990). The invariant dating service. Nature 348:581–582.

    PubMed  CAS  Google Scholar 

  100. Pieters, J., Bakke, O., and Dobberstein, B. (1993). The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 106:831–846.

    PubMed  CAS  Google Scholar 

  101. Roche, P. A., and Cresswell, P. (1990). Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345:615–618.

    PubMed  CAS  Google Scholar 

  102. Roche, P. A., and Cresswell, P. (1991). Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA 88:3150–3154.

    PubMed  CAS  Google Scholar 

  103. Ziegler, H. K., and Unanue, E. R. (1982). Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of antigen presentation of T cells. Proc. Natl. Acad. Sci. USA 79:175–178.

    PubMed  CAS  Google Scholar 

  104. Collins, D. S., Unanue, E. R., and Harding, C. V. (1991). Reduction of disulphide bonds within lysosomes is a key step in antigen processing. J. Immunol. 147:4054–4059.

    PubMed  CAS  Google Scholar 

  105. Vidard, L., Rock, K. L., and Benacerraf, B. (1991). The generation of immunogenic peptides can be selectively increased or decreased by proteolytic enzyme inhibitors. J. Immunol. 147:1786–1791.

    PubMed  CAS  Google Scholar 

  106. Mouritsen, S., Meldal, M., Werdelin, O., Stryhn Hansen, A., and Buus, S. (1992). MHC molecules protect T cell epitopes against proteolytic destruction. J. Immunol. 149:1987–1993.

    PubMed  CAS  Google Scholar 

  107. Amigorena, S., Drake, J. R., Webster, P., and Mellman, I. (1994). Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369:113–120.

    PubMed  CAS  Google Scholar 

  108. Tulp, A., Verwoerd, D., Dobberstein, B., Ploegh, H. L., and Pieters, J. (1994). Isolation and characterization of the intracellular MHC class II compartment. Nature 369:120–126.

    PubMed  CAS  Google Scholar 

  109. West, M. A., Lucocq, J. M., and Watts, C. (1994). Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature 369:147–151.

    PubMed  CAS  Google Scholar 

  110. Schmid, S. L., and Jackson, M. R. (1994). Making class II presentable. Nature 369:103–104.

    PubMed  CAS  Google Scholar 

  111. Germain, R. N., and Rinker, A. G. J. (1993). Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes surface expression of occupied molecules. Nature 363:725–728.

    PubMed  CAS  Google Scholar 

  112. Morris, P., Shaman, J., Attaya, M., Amaya, M., Goodman, S., Bergman, C., Moneo, J. J., and Mellins, E. (1994). An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368:551–553.

    PubMed  CAS  Google Scholar 

  113. Fling, S. P., Arp, B., and Pious, D. (1994). HLA-DMA and-DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells. Nature 368:554–558.

    PubMed  CAS  Google Scholar 

  114. Klatzmann, D., Champagne, E., Chamaret, S., Gruest, J., Guetard, D., Hercend, T., Gluckman, J. C., and Montagnier, L. (1984). T-lym-phocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312:767–768.

    PubMed  CAS  Google Scholar 

  115. De Rossi, A., Franchini, G., Aldovini, A., Del Mistro, A., Chieco-Bianchi, L., Gallo, R. C., and Wong-Staal, F. (1986). Differential response to the cytopathic effects of human T-cell lymphotrophic virus type III (HTLV-III) superinfection in T4+ (helper) and T8+ (suppressor) T-cell clones transformed by HTLV-I. Proc. Natl. Acad. Sci. USA 83:4297–4301.

    PubMed  Google Scholar 

  116. Folks, T., Kelly, J., Benn, S., Kinter, A., Justement, J., Gold, J., Redfield, R., Sell, K. W., and Fauci, A. S. (1986). Susceptibility of normal human lymphocytes to infection with HTLV-III/LAV. J. Immunol. 136:4049–4053.

    PubMed  CAS  Google Scholar 

  117. Lasky, L. A., Nakamura, G., Smith, D. H., Fennie, C., Shimasaki, C., Patzer, E., Berman, P., Gregory, T., and Capon, D. J. (1987). Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 50:975–985.

    PubMed  CAS  Google Scholar 

  118. Rudnick, G., and Clark, J. (1993). From synapse to vesicle: The reuptake and storage of biogenic amine neurotransmitter. Biochim. Biophys. Acta 1144:249–263.

    PubMed  CAS  Google Scholar 

  119. McMahon, A. T., and Nicholls, D. G. (1991). The bioenergetics of neurotransmitter release. Biochim. Biophys. Acta 1059:243–264.

    PubMed  CAS  Google Scholar 

  120. Maycox, P. R., Link, E., Reetz, A., Morris, S. A., and Jahn, R. (1992). Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118:1379–1388.

    PubMed  CAS  Google Scholar 

  121. Sudhof, T. C., and Jahn, R. (1991). Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6:665–677.

    PubMed  CAS  Google Scholar 

  122. Kelly, R. B. (1993). Storage and release of neurotransmitters. Cell (Suppl.) 72:43–53.

    PubMed  Google Scholar 

  123. Regnier-Vigoroux, A., and Huttner, W. B. (1994). Biogenesis of small synaptic vesicles and synaptic-like microvesicles. Neurochem. Res. 18:59–64.

    Google Scholar 

  124. Linstedt, A. D., and Kelly, R. B. (1991). Synaptophysin is sorted from endocytotic markers in neuroendocrine PC12 cells but not transfected fibroblasts. Neuron 7:309–317.

    PubMed  CAS  Google Scholar 

  125. Ceccarelli, B., Hurlbut, W. P., and Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junctions. J. Cell Biol. 57:499–524.

    PubMed  CAS  Google Scholar 

  126. Valtorta, F., Fesce, R., Grohovaz, F., Haimann, C., Hurlbut, W. P., Lezzi, H., Torri-Tarelli, F., Villa, A., and Ceccarelli, B. (1990). Neurotransmitter release and synaptic vesicle recycling. Neuroscience 35:477–489.

    PubMed  CAS  Google Scholar 

  127. Miller, T. M., and Heuser, J. E. (1984). Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J. Cell Biol. 98:685–698.

    PubMed  CAS  Google Scholar 

  128. Heuser, J. (1989). The role of coated vesicles in recycling of synaptic vesicle membrane. Cell Biol. Int. Rep. 13:1063–1076.

    PubMed  CAS  Google Scholar 

  129. Robinson, M. S. (1989). Cloning of cDNAs encoding two related 100-kD coated vesicle proteins (α-adaptins). J. Cell Biol. 108:833–842.

    PubMed  CAS  Google Scholar 

  130. Ponnambalam, S., Robinson, M. S., Jackson, A. P., Peiper, L., and Parham, P. (1993). Conservation and diversity in families of coated vesicle adaptins. J. Biol. Chem. 265:4814–4820.

    Google Scholar 

  131. Jackson, A. P., Sewo, H. F., Holmes, N., Drickamer, K., and Parhem, P. (1987). Clathrin light chains contain brain-specific insertion sequences and a region of homology with intermediate filaments. Nature 326:154–159.

    PubMed  CAS  Google Scholar 

  132. Pearse, B. M., and Robinson, M. S. (1990). Clathrin, adaptors and sorting. Annu. Rev. Cell Biol. 6:151–171.

    PubMed  CAS  Google Scholar 

  133. Haimann, C., Torri-Tarelli, F., Fesce, R., and Ceccarelli, B. (1985). Measurement of quantal secretion induced by ouabain and its correlation with depletion of synaptic vesicles. J. Cell Biol. 101:1953–1965.

    PubMed  CAS  Google Scholar 

  134. Bennett, M. V. L., Model, P. G., and Highstein, S. M. (1976). Stimulation-induced depletion of vesicles, fatigue of transmission and recovery processes at a vertebrate central synapse. Cold Spring Harbor Symp. Quant. Biol. 40:25–36.

    PubMed  CAS  Google Scholar 

  135. Sulzer, D., and Holtzman, E. (1989). Acidification and endosome-like compartments in the presynaptic terminals of frog retinal photoreceptors. J. Neurocytol. 18:529–540.

    PubMed  CAS  Google Scholar 

  136. Lassman, H., Weiler, R., Fischer, P., Bancher, C., Jellinger, K., Floor, E., Danielczyk, W., Seitelberger, F., and Winkler, H. (1992). Synaptic pathology in Alzheimer’s disease: Immunological data for markers of synaptic and large dense core vesicles. Neuroscience 46:1–8.

    Google Scholar 

  137. Lisak, R. P. (1994). Handbook of Myasthenia Gravis and Myasthenic Syndromes, Dekker, New York, pp. 81–102.

    Google Scholar 

  138. Leveque, C., Hoshino, T., David, P., Shoji-Kasai, Y, Leys, K., Omori, A., Lang, B., El Far, O., Sato, K., Martin, M. N., Newsom-Davis, J., Takahashi, M., and Seagar, M. (1992). The synaptic vesicle protein synaptotagmin associates with calcium channels and is a putative Lambert-Eaton myasthenic syndrome antigen. Proc. Natl. Acad. Sci. USA 89:3625–3629.

    PubMed  CAS  Google Scholar 

  139. Lichte, B., Veh, R. W., Meyer, H. E., and Kilimann, M. W. (1992). Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J. 11:2521.

    PubMed  CAS  Google Scholar 

  140. De Camilli, P., Thomas, A., Cofiel, R., Folli, F., Lichte, B., Piccolo, G., Meinck, H., Austoni, M., Fassetta, G., Bottazzo, G., Bates, D., Cartlidge, N., Solimena, M., and Kilimann, M. W. (1993). The synaptic vesicle-associated protein amphyphysin is the 128 kD au-toantigen of Stiff-Man Syndrome with breast cancer. J. Exp. Med. 178:2219–2223.

    PubMed  Google Scholar 

  141. Cadena, D. H., and Gill, G. N. (1992). Receptor tyrosine kinases. FASEB J. 6:2332–2337.

    PubMed  CAS  Google Scholar 

  142. Kahn, M. N., Lai, W. H., Burgess, J. W., Posner, B. I., and Bergeron, J. J. M. (1993). Potential role of endosomes in transmembrane signaling. In Subcellular Biochemistry. Endocytic Components: Identification and Characterization (J. J. M. Bergeron and J. R. Harris, eds.), Plenum Press, New York, pp. 223–254.

    Google Scholar 

  143. Fantl, W. J., Johnson, D. E., and Williams, L. T. (1993). Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62:453–481.

    PubMed  CAS  Google Scholar 

  144. Ullrich, A., and Schlessinger, J. (1990). Signal transduction by receptors with tyrosine kinase activity. Cell 61:203–212.

    PubMed  CAS  Google Scholar 

  145. Pazin, M. J., and Williams, L. T. (1992). Triggering signaling cascades by receptor tyrosine kinases. Trends Biochem. Sci. 17:374–378.

    PubMed  CAS  Google Scholar 

  146. Knutson, V. P., Ronnett, G. V., and Lane, M. D. (1985). The effects of cycloheximide and chloroquine on insulin receptor metabolism. Differential effects on receptor recycling and inactivation and insulin degradation. J. Biol. Chem. 260:14180–14188.

    PubMed  CAS  Google Scholar 

  147. Lai, W. H., Cameron, P. H., Wada, I., Doherty, J. J., Posner, B. I., and Bergeron, J. J. M. (1989). Ligand mediated internalization, recycling, and down regulation of the epidermal growth factor receptor in vivo. J. Cell Biol. 109:2741–2749.

    PubMed  CAS  Google Scholar 

  148. Duckworth, W. C., Hamel, F. G., Peavy, D. E., Liepnieks, J. J., Ryan, M. P., Hermodson, M. A., and Frank, B. H. (1988). Degradation products of insulin generated by hepatocytes and by insulin protease. J. Biol. Chem. 263:1826–1833.

    PubMed  CAS  Google Scholar 

  149. Knutson, V. P., Ronnett, G. V., and Lane, M. D. (1982). Control of insulin receptor level in 3T3 cells: Effect of insulin-induced down-regulation and dexamethasone-induced up-regulation on rate of receptor inactivation. Proc. Natl. Acad. Sci. USA 79:2822–2826.

    PubMed  CAS  Google Scholar 

  150. Ronnett, G. V., Knutson, V. P., and Lane, M. D. (1982). Insulin-induced down-regulation of insulin receptors in 3T3-L1 adipocytes. Altered rate of receptor inactivation. J. Biol. Chem. 257:4285–4291.

    PubMed  CAS  Google Scholar 

  151. Knutson, V. P., Ronnett, G. V., and Lane, M. D. (1983). Rapid, reversible internalization of cell surface insulin receptors. Correlation with insulin-induced down-regulation. J. Biol. Chem. 258:12139–12142.

    PubMed  CAS  Google Scholar 

  152. Burgess, J. W., Wada, I., Ling, N., Kahn, M. N., Bergeron, J. J. M., and Posner, B. I. (1992). Decrease in β-subunit phosphotyrosine correlates with internalization and activation of the insulin receptor kinase. J. Biol. Chem. 267:10077–10086.

    PubMed  CAS  Google Scholar 

  153. Backer, J. M., Kahn, C. R., and White, M. F. (1989). Tyrosine phosphorylation of the insulin receptor during insulin-stimulated internalization in rat hepatoma cells. J. Biol. Chem. 264:1694–1701.

    PubMed  CAS  Google Scholar 

  154. King, M. J., and Sale, G. J. (1990). Dephosphorylation of insulin-receptor autophosphorylation sites by particulate and soluble phos-photyrosyl-protein phosphatases. Biochem. J. 266:251–259.

    PubMed  CAS  Google Scholar 

  155. Faure, R., Baquiran, G., Bergeron, J. J. M., and Posner, B. I. (1992). The dephosphorylation of insulin and epidermal growth factor receptors: Role of endosome-associated phosphotyrosine phosphatase(s). J. Biol. Chem. 267:11215–11221.

    PubMed  CAS  Google Scholar 

  156. Posner, B. I., Patel, B., Verma, A. K., and Bergeron, J. J. M. (1980). Uptake of insulin by plasmalemma and Golgi subcellular fractions of rat liver. J. Biol. Chem. 255:735–741.

    PubMed  CAS  Google Scholar 

  157. Sorkin, A., Waters, C., Overholser, K. A., and Carpenter, G. (1991). Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J. Biol. Chem. 266:8355–8362.

    PubMed  CAS  Google Scholar 

  158. Felder, S., LaVin, J., Ullrich, A., and Schlessinger, J. (1992). Kinetics of binding, endocytosis and recycling of EGF receptor mutants. J. Cell Biol. 117:203–212.

    PubMed  CAS  Google Scholar 

  159. Carpentier, J.-L., Paccaud, J.-P., Backer, J., Gilbert, A., Orci, L., and Kahn, C. R. (1993). Two steps of insulin internalization depend on different domains of the β subunit. J. Cell Biol. 122:1243–1252.

    PubMed  CAS  Google Scholar 

  160. McClain, D. A., Maegawa, H., Lee, J., Dull, T. J., Ullrich, A., and Olefsky, J. M. (1987). A mutant insulin receptor with defective tyrosine kinase displays no biologic activity and does not undergo endocytosis. J. Biol. Chem. 262:14663–14671.

    PubMed  CAS  Google Scholar 

  161. Chou, C. K., Dull, T. J., Russell, D. S., Cherzi, R., Lebwohl, D., Ullrich, A., and Rosen, O. M. (1987). Human insulin receptor mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J. Biol. Chem. 262:1842–1847.

    PubMed  CAS  Google Scholar 

  162. Ebina, Y, Araki, E., Taira, M., Shimada, R., Mori, M., Craik, C. S., Siddle, K., Pierce, S. B., Roth, R. A., and Rutter, W. J. (1987). Replacement of lysine residue 1030 in the putative ATP-binding region of the insulin receptor abolishes insulin-and antibody-stimulated glucose uptake and receptor kinase activity. Proc. Natl. Acad. Sci. USA 84:704–708.

    PubMed  CAS  Google Scholar 

  163. Honegger, A. M., Dull, T. J., Felder, S., Van Obberghen, E., Bellot, F, Szapary, D., Schmidt, A., Ullrich, A., and Schlessinger, J. (1987). Point mutation at the ATP binding site of EGF receptor abolishes protein-tyrosine kinase activity and alters cellular routing. Cell 51:199–209.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  165. Iwashita, S., and Kobayashi, M. (1992). Signal transduction system for growth factor receptors associated with tyrosine kinase activity: Epidermal growth factor receptor signalling and its regulation. Cell. Signal. 4:123–132.

    PubMed  CAS  Google Scholar 

  166. Crouch, M. F., and Hendry, I. A. (1993). Growth factor second messenger systems: Oncogenes and the heterotrimeric GTP-binding protein connection. Med. Res. Rev. 13:105–123.

    PubMed  CAS  Google Scholar 

  167. Chen, W. S., Lazar, C. S., Lund, K. A., Welsh, J. B., Chang, C.-P., Walton, G. M., Oer, C. J., Wiley, H. S., Gill, G. N., and Rosenfeld, M. G. (1989). Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation. Cell 59:33–43.

    PubMed  CAS  Google Scholar 

  168. Knutson, V. P., Donnelly, P. V., Balba, Y., et al. (1995). Insulin resistance mediated by a proteolytic fragment of the insulin receptor. J. Biol. Chem. 270:24972–24981.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, University of Texas-Houston Medical School, Houston, Texas, 77225, USA

    Victoria P. Knutson, Patricia V. Donnelly, Maria M. Lopez-Reyes & Yvonne L. O. Balba

Authors
  1. Victoria P. Knutson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia V. Donnelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria M. Lopez-Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yvonne L. O. Balba
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of Texas Medical School at Houston, Houston, Texas, USA

    Stanley G. Schultz

  2. University of Arkansas College of Medicine, Little Rock, Arkansas, USA

    Thomas E. Andreoli

  3. Case Western Reserve University, Cleveland, Ohio, USA

    Arthur M. Brown

  4. The Johns Hopkins University, Baltimore, Maryland, USA

    Douglas M. Fambrough

  5. Yale University School of Medicine, New Haven, Connecticut, USA

    Joseph F. Hoffman

  6. University of Iowa College of Medicine, Iowa City, Iowa, USA

    Michael J. Welsh

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Plenum Press, New York

About this chapter

Cite this chapter

Knutson, V.P., Donnelly, P.V., Lopez-Reyes, M.M., Balba, Y.L.O. (1996). Receptor-Mediated Endocytosis. In: Schultz, S.G., Andreoli, T.E., Brown, A.M., Fambrough, D.M., Hoffman, J.F., Welsh, M.J. (eds) Molecular Biology of Membrane Transport Disorders. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-1143-0_16

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-1143-0_16

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8446-8

  • Online ISBN: 978-1-4613-1143-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation