Compartments of the Early Secretory Pathway

  • Rob J. M. Hendriks
  • Stephen D. Fuller
Part of the Subcellular Biochemistry book series (SCBI, volume 22)


The secretory pathway consists of a set of compartments responsible for the assembly and modification of proteins destined for secretion, for transport to the plasma membrane, and to the other organelles of the cell. The classical description of the secretory pathway comprises the endoplasmic reticulum (ER) as the site of protein synthesis and first maturation steps, and the Golgi apparatus as the site of protein modification and sorting. Apart from synthesis and maturation of secreted proteins the pathway is also responsible for the production of its own components. Hence, the enzymes and factors involved in the functions of the pathway are continually renewed and are being transported to their positions within the pathway by the machinery that transports secretory proteins through it. It is this latter aspect of the pathway, its mechanism of self-renewal, that complicates both the definition and the description of the compartments of the secretory pathway. In this review we will adopt a functional approach to the description of the components of the early secretory pathway and focus on its dynamic aspects. Here the ER will be referred to as the aggregate of smooth ER (sER), rough ER (rER), and the nuclear envelope that is continuous with them. The Golgi is defined as the aggregate of cisterna and connected networks on both the trans (TGN, trans-Golgi network) and cis (CGN, cis-Golgi network) sides. We will focus on membrane traffic between the ER and Golgi compartment and will present a useful framework for understanding the membrane traffic that gives rise to these compartments.


Endoplasmic Reticulum Secretory Pathway Golgi Complex Vesicular Stomatitis Virus Transport Vesicle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alberini, C. M., Bet, P., Milstein, C., and Sitia, R., 1990, Secretion of immunoglobulin M assembly intermediates in the presence of reducing agents, Nature 347:485–487.PubMedCrossRefGoogle Scholar
  2. Amar-Costesec, A., Todd, J. A., and Kreibich, G., 1984, Segregation of the Polypeptide translocation apparatus to regions of the endoplasmic reticulum containing ribophorins and ribosomes. I: Functional tests on rat liver microsomal subfractions, J. Cell Biol. 99:2247–2253.PubMedCrossRefGoogle Scholar
  3. Amara, J. F., Lederkremer, G., and Lodish, H. F., 1989, Intracellular degradation of unassembled asialoglycoprotein receptor subunits: A pre-Golgi nonlysosomal endoproteolytic cleavage, J. Cell Biol. 110:3315–3324.CrossRefGoogle Scholar
  4. Armstrong, J., Patel, S., and Riddle, P., 1990, Lysosomal sorting mutants of Coronavirus El protein, a Golgi membrane protein, J. Cell Sci. 95:191–197.PubMedGoogle Scholar
  5. Baker, D., Hicke, L., Rexach, M., Schleyer, M., and Schekman, R., 1988, Reconstitution of SEC gene product-dependent intercompartmental protein transport, Cell 54:335–344.PubMedCrossRefGoogle Scholar
  6. Balch, W., 1992, From G minor to G major, Current Biology 2:157–169.PubMedCrossRefGoogle Scholar
  7. Balch, W., Elliot, M., and Keller, D., 1986, ATP coupled transport of vesicular stomatitis virus G protein between the endoplasmic reticulum and the Golgi apparatus, J. Biol. Chem. 261:14681–14689.PubMedGoogle Scholar
  8. Bardeletti, G., Tektoff, J., and Gautheron, D., 1979, Rubella virus maturation and production in two host cell systems, Intervirology 11:97–103.PubMedCrossRefGoogle Scholar
  9. Beckers, C. J. M., and Balch, W. E., 1989, Calcium and GTP: Essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus, J. Cell Biol. 108:1245–1256.PubMedCrossRefGoogle Scholar
  10. Berger, M., and Schmidt, M. F. 1985, Protein fatty acyltransferase is located in the rough endoplasmic reticulum, FEBS Lett. 187:289–294.PubMedCrossRefGoogle Scholar
  11. Bergman, L. W., and Kuehl, W. M., 1979, Formation of an intrachain disulfide bond on nascent immunoglobulin light chains, J. Biol. Chem. 254:8869–8876.PubMedGoogle Scholar
  12. Bergmann, C. C., Maass, D., Poruchynsky, M. S., Atkinson, P. H., and Bellamy, A. R., 1989, Topology of the non-structural rotavirus receptor glycoprotein NS28 in the rough endoplasmic reticulum, EMBO J. 8:1695–1703.PubMedGoogle Scholar
  13. Bergmann, J. E., and Fusco, P. J., 1990, The G protein of vesicular stomatitis virus has free access into and egress from the smooth endoplasmic reticulum of UT-1 cells, J. Cell Biol. 110:625–635.PubMedCrossRefGoogle Scholar
  14. Bonatti, S., Migliaccio, G., and Simons, K., 1989, Palmitoylation of viral membrane glycoproteins takes place after exit from the endoplasmic reticulum, J. Biol Chem. 264:12590–12595.PubMedGoogle Scholar
  15. Bonifacino, J., and Lippincott-Schwartz, J., 1991, Degradation of proteins within the endoplasmic reticulum, Curr. Opin. Cell Biol. 3:592–600.PubMedCrossRefGoogle Scholar
  16. Bonifacino, J. S., Cosson, P., Shah, N., and Klausner, R. D., 1991, Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum, EMBO J. 10:2783–2793.PubMedGoogle Scholar
  17. Booth, C., and Koch, G. L., 1989, Perturbation of cellular calcium induces secretion of luminal ER proteins, Cell 59:729–737.PubMedCrossRefGoogle Scholar
  18. Braakman, I., Helenius, J., and Helenius, A., 1992a, Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum, EMBO J. 11:1717–1722.PubMedGoogle Scholar
  19. Braakman, I., Helenius, J., and Helenius, A., 1992b, Role of ATP and disulphide bonds during protein folding in the endoplasmic reticulum, Nature 356:260–262.PubMedCrossRefGoogle Scholar
  20. Braakman, I., Hoover-Litty, H., Wagner, K. R., and Helenius, A., 1991, Folding of influenza hemagglutinin in the endoplasmic reticulum, J. Cell Biol. 114:401–411.PubMedCrossRefGoogle Scholar
  21. Buonocore, L., and Rose, J. K., 1990, Prevention of HIV-1 glycoprotein transport by soluble CD4 retained in the endoplasmic reticulum, Nature 345:625–628.PubMedCrossRefGoogle Scholar
  22. Burgess, T. L., and Kelly, R. B., 1987, Constitutive and regulated secretion of proteins, Annu. Rev. Cell Biol. 3:243–293.PubMedCrossRefGoogle Scholar
  23. Burgoyne, R. D., Cheek, T. R., Morgan, A., O’Sullivan, A. J., Moreton, R. B., Berridge, M. J., Mata, A. M., Colyer, J., Lee, A. G., and East, J. M., 1989, Distribution of two distinct Ca-ATPase likie proteins and their relationship to the agonist-sensitive calcium store in adrenal chromaffin cells, Nature 342:12–14.Google Scholar
  24. Ceriotti, A., and Colman, A., 1988, Binding to membrane proteins within the endoplasmic reticulum cannot explain the retention of the glucose-regulated protein GRP78 in Xenopus oocytes, EMBO J. 7:633–638.PubMedGoogle Scholar
  25. Chau, V., Tobias, J., Bachmair, A., Marriot, D., Echer, D., Gonda, D., and Varshavsky, A., 1989, A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein, Science 243:1576–1583.PubMedCrossRefGoogle Scholar
  26. Chavrier, P., Parton, R. G., Hauri, H. P., Simons, K., and Zerial, M., 1990, Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments, Cell 62:317–329.PubMedCrossRefGoogle Scholar
  27. Chege, N., and Pfeffer, S., 1990, Compartmentalization of the Golgi complex: Brefeldin A distinguishes trans-Golgi cisternae from the trans-Golgi network, J. Cell Biol. 111:893–899.PubMedCrossRefGoogle Scholar
  28. Clary, D. O., Griff, I. C., and Rothman, J. E., 1990, SNAPS, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast, Cell 61:709–721.PubMedCrossRefGoogle Scholar
  29. Cosson, P., Lankford, S. P., Bonifacino, J. S., and Klausner, R. D., 1991, Membrane protein association by potential intramembrane charge pairs, Nature 351:414–416.PubMedCrossRefGoogle Scholar
  30. Crimaldo, C., Hortsch, M., Gausepohl, H., and Meyer, D., 1987, Human ribophorins I and II: The primary structure and membrane topology of two highly conserved rough endoplasmic reticulum-specific glycoproteins, EMBO J. 6:75–82.Google Scholar
  31. Dean, N., and Pelham, H. R., 1990, Recycling of proteins from the Golgi compartment to the ER in yeast, J. Cell Biol. 111:369–377.PubMedCrossRefGoogle Scholar
  32. Doms, R. W., Keller, D. S., Helenius, A., and Balch, W. E., 1987, Role for adenosine tri-phosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers, J. Cell Biol. 105:1957–1969.PubMedCrossRefGoogle Scholar
  33. Doms, R. W., Russ, W. G., and Yewdell, J. W., 1989, Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum, J. Cell Biol. 109:61–72.PubMedCrossRefGoogle Scholar
  34. Doms, R. W., Ruusala, A., Machamer, C., Helenius, J., Helenius, A., and Rose, J. K., 1988, Differential effects of mutations in three domains on folding, quaternary structure, and intracellular transport of vesicular stomatitis virus G protein, J. Cell Biol. 107:89–99.PubMedCrossRefGoogle Scholar
  35. Donaldson, J., Finazzi, D., and Klausner, R., 1992, Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein, Nature 360:350–352.PubMedCrossRefGoogle Scholar
  36. Downes, C. S., Musk, S. R. R., Watson, J. V., and Johnson, R. T., 1990, Caffeine overcomes a restriction point associated with DNA replication but does not accelerate mitosis, J. Cell Biol. 110:1855–1859.PubMedCrossRefGoogle Scholar
  37. Doyle, C., Roth, M. G., Sambrook, J., and Gething, M.-J., 1985, Mutations in the cytoplasmic domain of the influenza virus hemagglutinin affect different stages of intracellular transport, J. Cell Biol. 100:704–714.PubMedCrossRefGoogle Scholar
  38. Doyle, C., Sambrook, J., and Gething, M.-J., 1986, Analysis of progressive deletions of the transmembrane and cytoplasmic domains of influenza hemagglutinin, J. Cell Biol. 103:1193–1204.PubMedCrossRefGoogle Scholar
  39. Duden, R., Allan, V., and Kreis, T., 1991a, Involvement of β-COP in membrane traffic through the Golgi complex, Trends Cell Biol. 1:14–19.PubMedCrossRefGoogle Scholar
  40. Duden, R., Griffiths, G., Frank, R., Argos, P., and Kreis, T., 1991b, β-COP, 110kD protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to β-adaptin, Cell 64:649–665.PubMedCrossRefGoogle Scholar
  41. Dunphy, W. G., Fries, E., Urbani, L. J., and Rothman, J. E., 1981, Early and late functions associated with the Golgi apparatus reside in distinct compartments, Proc. Natl. Acad. Sci. USA 78:7453–7457.PubMedCrossRefGoogle Scholar
  42. Estes, M. K., 1990, Rotaviruses and their replication, in Virology, pp. 1329–1352, Raven Press, New York.Google Scholar
  43. Estes, M. K., and Cohen, J., 1989, Rotavirus gene structure and function, Microbiol Rev 53:410–449.PubMedGoogle Scholar
  44. Fawcett, D. W., 1981, The Cell, 2nd ed., pp. 332–333, W. B. Saunders, Philadelphia.Google Scholar
  45. Fine, R. E., 1989, Vesicles without clathrin: Intermediates in bulk flow exocytosis, Cell 58:609–610.PubMedCrossRefGoogle Scholar
  46. Flynn, G. C., Chappell, T. G., and Rothman, J. E., 1989, Peptide binding and release by proteins implicated as catalysts of protein assembly, Science 245:385–390.PubMedCrossRefGoogle Scholar
  47. Freedman, R., 1987, Folding into the right shape, Nature 329:196–197.PubMedCrossRefGoogle Scholar
  48. Freedman, R., and Hillson, D., 1980, Formation of disulphide bonds, in The Enzymology of Post-translational modification (R. Freedman and H. Hawkins, eds.), Academic Press, London.Google Scholar
  49. Freedman, R. B., 1984, Native disulphide bond formation in protein biosynthesis: Evidence for the role of protein disulphide isomerase, Trends Biochem. Sci. 9:438–441.CrossRefGoogle Scholar
  50. Fujiwara, T., Oda, K., Yokota, A., Takatsuki, A., and Ikehara, Y., 1988, Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum, J. Biol. Chem. 265:18545–18552.Google Scholar
  51. Fuller, S. D., 1987, The T-4 envelope of Sindbis virus is organized by interactions with a complementary T-3 capsid, Cell 48:923–934.PubMedCrossRefGoogle Scholar
  52. Fuller, S. D., Vriend, G., Pastore, A., and Eder, A., 1993, A model for the structure of the KDEL ER retention sequence leads to a model of environment dependent recognition, in preparation.Google Scholar
  53. Gallagher, P., Henneberry, J., Wilson, I., Sambrook, J., and Gething, M.-J., 1988, Addition of carbohydrate side chains at novel sites on influenza virus hemagglutinin can modulate the folding, transport, and activity of the molecule, J. Cell Biol. 107:2059–2073.PubMedCrossRefGoogle Scholar
  54. Galteau, M. M., Antoine, B., and Reggio, H., 1985, Epoxide hydrolase is a marker for the smooth endoplasmic reticulum in rat liver, EMBO J. 4:2793–2800.PubMedGoogle Scholar
  55. Ganem, D., 1991, Assembly of hepadnaviral virions and subviral particles, Curr. Top. Microbiol. Immunol. 168:61–83.PubMedCrossRefGoogle Scholar
  56. Ganem, D., and Varmus, H., 1987, The molecular biology of hepatitis B viruses, Annu. Rev. Biochem. 56:561–693.CrossRefGoogle Scholar
  57. Geetha-Habib, M., Noiva, R., Kaplan, H. A., and Lennarz, W. J., 1988, Glycosylation site binding protein, a component of oligosaccharyl transferase, is highly similar to three other 57-kd luminal proteins of the ER, Cell 54:1053–1060.PubMedCrossRefGoogle Scholar
  58. Gerace, L., Comeau, C., and Benson, M., 1984, Organization and modulation of nuclear lamina structure, J. Cell Sci. (Suppl.) 1:137–160.Google Scholar
  59. Gething, M.-J., McCammon, K., and Sambrook, J., 1986, Expression of wild-type and mutant forms of influenza hemagglutinin: The role of folding in intracellular transport, Cell 46:939–950.PubMedCrossRefGoogle Scholar
  60. Gething, M.-J., and Sambrook, J., 1990, Transport and assembly processes in the endoplasmic reticulum, Semin. Cell Biol. 1:65–72.PubMedGoogle Scholar
  61. Görlich, D., Hartmann, E., Prehn, S., and Rapoport, T. A., 1992, A protein of the endoplasmic reticulum involved early in Polypeptide translocation, Nature 357:47–52.PubMedCrossRefGoogle Scholar
  62. Görlich, D., Prehn, S., Hartmann, E., Herz, J., Otto, A., Kraft, R., Wiedman, M., Knepsel, S., Dobberstein, B., and Rapoport, T.A., 1990, The signal sequence receptor has a second subunit and is part of a translocation complex in the endoplasmic reticulum as probed by bifunctional reagents, J. Cell Biol. 111:2283–2294.PubMedCrossRefGoogle Scholar
  63. Goud, B., 1992, Small GTP binding proteins as compartmental markers, Semin. Cell Biol. 3:301–307.PubMedCrossRefGoogle Scholar
  64. Griffiths, G., Fuller, S. D., Back, R., Hollinshead, M., Pfeiffer, S., and Simons, K., 1989, The dynamic nature of the Golgi complex, J. Cell Biol. 108:277–297.PubMedCrossRefGoogle Scholar
  65. Griffiths, G., and Rottier, P., 1992, Cell biology of viruses that assemble along the biosynthetic pathway, Semin. Cell Biol. 3:367–381.PubMedCrossRefGoogle Scholar
  66. Griffiths, G., and Simons, K., 1986, The trans-Golgi network: Sorting at the site of exit from the Golgi complex, Science 234:438–443.PubMedCrossRefGoogle Scholar
  67. Hardwick, K. G., Lewis, M. J., Semenza, J., Dean, N., and Pelham, H. R., 1990, ERD1, a yeast gene required for the retention of luminal endoplasmic reticulum proteins, affects glycoprotein processing in the Golgi apparatus, EMBO J. 9:623–630.PubMedGoogle Scholar
  68. Hauri, H.-P., and Schweizer, A., 1992, The endoplasmic reticulum-Golgi intermediate compartment, Curr. Opin. Cell Biol. 4:600–608.PubMedCrossRefGoogle Scholar
  69. Hearing, J., Gething, M.-J., and Sambrook, J., 1989, Addition of truncated Oligosaccharides to influenza virus hemagglutinin results in its temperature-conditional cell-surface expression, J. Cell Biol. 108:355–365.PubMedCrossRefGoogle Scholar
  70. Helms, J., and Roth man, J., 1992, Inhibition by Brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF, Nature 360:352–354.PubMedCrossRefGoogle Scholar
  71. High, S., and Dobberstein, B., 1992, Mechanisms that determine the transmembrane disposition of proteins, Curr. Opin. Cell Biol. 4:581–586.PubMedCrossRefGoogle Scholar
  72. Hobman, T. C., Lundstrom, M. E., and Gillam, S., 1990, Processing and transport of rubella virus structural proteins in COS cells, Virology 178:122–133.PubMedCrossRefGoogle Scholar
  73. Hobman, T. C., Woodward, L., and Farquhar, M. G., 1992, The rubella virus El glycoprotein is arrested in a novel post-ER, pre-Golgi compartment, J. Cell Biol. 118:795–811.PubMedCrossRefGoogle Scholar
  74. Hortsch, M., and Meyer, D. I., 1985, Immunochemical analysis of rough and smooth microsomes from rat liver: Segregation of docking protein in rough membranes, Eur. J. Biochem. 150:559–564.PubMedCrossRefGoogle Scholar
  75. Hsu, V. W., Shah, N., and Klausner, R. D., 1992, A Brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1, Cell 69:625–635.PubMedCrossRefGoogle Scholar
  76. Hsu, V. W., Yuan, L. C., Nuchtern, J. G., Lippincott-Schwarz, J., Hammerling, G. J., and Klausner, R. D., 1991, A recycling pathway between the endoplasmic reticulum and the Golgi apparatus for retention of unassembled MHC class I molecules, Nature 352:441–444.PubMedCrossRefGoogle Scholar
  77. Hughson, E., Wandinger-Ness, A., Gausepohl, H., Griffiths, G., and Simons, K., 1988, The cell biology of enveloped virus infection of epithelial tissues, in Molecular Biology and Infectious Diseases, pp. 75–89, Elsevier, Paris.Google Scholar
  78. Huovila, A.-P., Eder, A., and Fuller, S., 1992, Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment, J. Cell Biol. 118:1305–1320.PubMedCrossRefGoogle Scholar
  79. Huovila, A.-P., and Fuller, S., 1993, An ER-Goigi intermediate compartment is not continuous with endoplasmic reticulum, submitted.Google Scholar
  80. Hurtley, S. M., Bole, D. G., Hoover, L. H., Helenius, A., and Copeland, C. S., 1989, Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP), J. Cell Biol. 108:2117–2126.PubMedCrossRefGoogle Scholar
  81. Hurtley, S. M., and Helenius A., 1989, Protein oligomerization in the endoplasmic reticulum, Annu. Rev. Cell Biol. 5:271–301.CrossRefGoogle Scholar
  82. Hwang, C., Sinskey, A., and Lodish, H., 1992, The oxidized redox potential in the endoplasmic reticulum: Glutathione as the principal redox buffer, Science 257:1496–1502.PubMedCrossRefGoogle Scholar
  83. Ivessa, N., De Lemos-Chiarandini, C., Tsao, Y., Takatsuki, A., Adesnik, M., Savatini, D., and Kreibich, G., 1992, O-glycosylation of intact and truncated ribophorins in Brefeldin A-treated cells: Newly synthesized ribophorins are only transiently accessible to the relocated gly-cosyltransferases, J. Cell Biol. 117:949–958.PubMedCrossRefGoogle Scholar
  84. Jackson, M. R., Nilsson, T., and Peterson, P. A., 1990, Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum, EMBO J. 9:3153–3162.PubMedGoogle Scholar
  85. Jones, A. L., and Fawcett, D. W., 1966, Hypertrophy of the agranular endoplasmic reticulum in hamster liver induced by phenobarbital, J. Histochem. Cytochem. 14:215–232.PubMedCrossRefGoogle Scholar
  86. Kabcenell, A. K., and Atkinson, P. H., 1985, Processing of the rough endoplasmic reticulum membrane glycoprotein of rotavirus SAH, J. Cell Biol. 101:1270–1280.PubMedCrossRefGoogle Scholar
  87. Kabcenell, A. K., Poruchynsky, M. S., Bellamy, A. R., Greenberg, H. B., and Atkinson, P. H., 1988, Two forms of VP7 are involved in the assembly of SA11 rotavirus in the endoplasmic reticulum, J. Virol. 62:2929–2941.PubMedGoogle Scholar
  88. Kaiser, C. A., and Schekman, R., 1990, Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway, Cell 61:723–733.PubMedCrossRefGoogle Scholar
  89. Kassenbrock, C. K., and Kelly, R. B., 1989, Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides, EMBO J. 8:1461–1467.PubMedGoogle Scholar
  90. Klausner, R., Donaldson, J., and Lippincott-Schwartz, J., 1992, Brefeldin A: Insights into the control of membrane traffic and organelle structure, J. Cell Biol. 116:1071–1080.PubMedCrossRefGoogle Scholar
  91. Klausner, R., and Sitia, R., 1990, Protein degredation in the endoplasmic reticulum, Cell 62:611–614.PubMedCrossRefGoogle Scholar
  92. Klausner, R. D., Lippincott-Schwartz, J., and Bonifacino, J. S., 1990, The T-cell antigen receptor: Insights into organelle biology, Annu. Rev. Cell Biol. 6:403–431.PubMedCrossRefGoogle Scholar
  93. Kleijmeer, M. J., Kelly, A., Geuze, H. J., Slot, J. W., Townsend, A., and Trowsdale, J., 1992, Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi, Nature 357:342–344.PubMedCrossRefGoogle Scholar
  94. Koch, G. L. E., Booth, C., and Wooding, F. B. P., 1988, Dissociation and reassembly of the endoplasmic reticulum in live cells, J. Cell Sci. 91:511–522.PubMedGoogle Scholar
  95. Kornfeld, R., and Kornfeld, S., 1985, Assembly of asparagine linked Oligosaccharides, Annu. Rev. Biochem. 54:631–664.PubMedCrossRefGoogle Scholar
  96. Kreibich, G. B., Ulrich, L., and Sabatini, D., 1978, Proteins of the rough endosomal membrane related to ribosome binding. I: Identification of ribophorins I and II, membranes characteristic of rough microsomes, J. Cell Biol. 77:464–487.PubMedCrossRefGoogle Scholar
  97. Krijnse-Locker, J., Rose, J. K., Horzinek, M. C., and Rottier, P. J. M., 1992, Membrane assembly of the triple-spanning Coronavirus M protein: Individual transmembrane domains show preferred orientation, J. Biol. Chem. 267:21911–21918.Google Scholar
  98. Kuismanen, E., Jäntti, J., Mäkiranti, V., and Sariola, M., 1992, Effect of caffeine on intracellular transport of Semliki Forest virus membrane glycoproteins, J. Cell Sci. 102:505–513.PubMedGoogle Scholar
  99. Kuismanen, E., and Saraste, J., 1989, Low temperature-induced transport blocks as tools to manipulate membrane traffic, Meth. Cell Biol. 32:257–274.CrossRefGoogle Scholar
  100. Lahtinen, U., Dahllöf, B., and Saraste, J., 1992, Characterization of a 58 kD cis-Golgi protein in pancreatic exocrine cells, J. Cell Sci. 103:321–333.PubMedGoogle Scholar
  101. Le, A., Graham, K. S., and Sifers, R. N., 1990, Intracellular degradation of the transport-impaired human PiZ a,-antitrypsin variant, J. Biol. Chem. 265:14001–14007.PubMedGoogle Scholar
  102. Lederkremer, G. Z., and Lodish, H. F., 1991, An alternatively spliced miniexon alters the subcellu-lar fate of the human asialoglycoprotein receptor H2 subunit: Endoplasmic reticulum retention and degradation or cell surface expression, J. Biol. Chem. 266:1237–1244.PubMedGoogle Scholar
  103. Lewis, M. J., and Pelham, H. R. B., 1990, A human homologue of the yeast HDEL receptor, Nature 348:162–163.PubMedCrossRefGoogle Scholar
  104. Lewis, M. J., and Pelham, H. R. B., 1992, Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum, Cell 68:353–364.PubMedCrossRefGoogle Scholar
  105. Lewis, M. J., Sweet, D. J., and Pelham, H. R., 1990, The ERD2 gene determines the specificity of the luminal ER protein retention system, Cell 61:1359–1363.PubMedCrossRefGoogle Scholar
  106. Lippincott-Schwartz, J., Bonifacino, J. C., Yuan, L. C., and Klausner, R. D., 1988, Degradation from endoplasmic reticulum: Disposing of newly synthesized proteins, Cell 54:209–220.PubMedCrossRefGoogle Scholar
  107. Lippincott-Schwartz, J., Donaldson, J. G., Schweizer, A., Berger, E. G., Hauri, H.-P., Yuan, L. C., and Klausner, R. D., 1990, Microtubule-dependent retrograde transport of proteins into the ER in the presence of Brefeldin A suggests an ER recycling pathway, Cell 60:821–836.PubMedCrossRefGoogle Scholar
  108. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S., and Klausner, R. D., 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.PubMedCrossRefGoogle Scholar
  109. Lodish, H. F., Kong, N., Snider, M., and Strous, G. J., 1983, Hepatoma secretory proteins migrate from rough endoplasmic reticulum to Golgi at characteristic rates, Nature 304:80–83.PubMedCrossRefGoogle Scholar
  110. Lotti, L. V., Torrisi, M.-R., Pascale, M. C., and Bonatti, S., 1992, Immunocytochemical analysis of the transfer of vesicular stomatitis virus G glycoprotein from the intermediale compartment to the Golgi complex, J. Cell Biol. 118:43–50.PubMedCrossRefGoogle Scholar
  111. Machamer, C. E., Mentone, S. A., Rose, J. K., and Farquhar, M. G., 1990, The El glycoprotein of an avian Coronavirus is targeted to the cis Golgi complex, Proc. Natl. Acad. Sci. USA 87:6944–6948.PubMedCrossRefGoogle Scholar
  112. Marquardt, T., and Helenius, A., 1992, Misfolding and aggregation of newly synthesized proteins in the endoplasmic reticulum, J. Cell Biol. 117:505–513.PubMedCrossRefGoogle Scholar
  113. Mazzarella, R. A., and Green, M., 1987, ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp90) and the 94-kDa glucose-regulated protein (GRP94), J. Biol. Chem. 260:6926–6931.Google Scholar
  114. Mellman, I., and Simons, K., 1992, The Golgi complex: In vitro veritas, Cell 68:829–840.PubMedCrossRefGoogle Scholar
  115. Meyer, D. I., and Dobberstein, B., 1980a, Identification and characterization of a membrane component essential for the translocation of nascent proteins across the membrane of the endoplasmic reticulum. J. Cell Biol. 87:503–508.PubMedCrossRefGoogle Scholar
  116. Meyer, D. I., and Dobberstein, B., 1980b, A membrane component essential for vectorial translocation of nascent proteins across the endoplasmic reticulum: Requirements for its extraction and reassociation with the membrane, J. Cell Biol. 87:498–502.PubMedCrossRefGoogle Scholar
  117. Meyer, D. I., Krause, E., and Dobberstein, B., 1982, Secretory protein translocation across membranes—the role of the “docking protein,” Nature 297:647–650.PubMedCrossRefGoogle Scholar
  118. Meyer, J. C, Bergmann, C. C., and Bellamy, A. R., 1989, Interaction of rotavirus cores with the nonstructural glycoprotein NS28, Virology 171:98–107.PubMedCrossRefGoogle Scholar
  119. Mundy, D., and Warren, G., 1992, Mitosis and inhibition of intracellular transport stimulate pal-mitoylation of a 62kD protein, J. Cell Biol. 116:135–146.PubMedCrossRefGoogle Scholar
  120. Munro, S., and Pelham, H. R., 1987, A C-terminal signal prevents secretion of luminal ER proteins, Cell 48:899–907.PubMedCrossRefGoogle Scholar
  121. Munro, S., and Pelham, H. R. B., 1986, An hsp70-like protein in the ER: Identity with the 78 kD glucose regulated protein and immunoglobulin heavy chain binding protein, Cell 46:291–300.PubMedCrossRefGoogle Scholar
  122. Navarro, D., Qadri, I., and Pereira, L., 1991, A mutation in the ectodomain of herpes simplex virus 1 glycoprotein B causes defective processing and retention in the endoplasmic reticulum, Virology 184:253–264.PubMedCrossRefGoogle Scholar
  123. Newman, A. P., and Ferro-Novick, S., 1987, Characterization of new mutants in the early part of the yeast secretory pathway isolated by a [3H]mannose suicide selection, J. Cell Biol. 105:1587–1594.PubMedCrossRefGoogle Scholar
  124. Nilsson, T., Jackson, M., and Peterson, P. A., 1989, Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum, Cell 58:707–718.PubMedCrossRefGoogle Scholar
  125. Novick, P., Field, C., and Schekman, R., 1980, Identification of 23 complementation groups required for post-translational events in the yeat’s secretory pathway, Cell 21:205–215.PubMedCrossRefGoogle Scholar
  126. Nuchtern, J. G., Bonifacino, J. S., Biddison, W. E., and Klausner, R. D., 1989, Brefeldin A implicates egress from endoplasmic reticulum in class I restricted antigen presentation, Nature 339:223–226.PubMedCrossRefGoogle Scholar
  127. Nunnari, J., and Walter, P., 1992, Protein targeting to and translocation across the membrane of the endoplasmic reticulum, Curr. Opin. Cell Biol. 4:573–580.PubMedCrossRefGoogle Scholar
  128. Oker-Blom, C., Kakkinen, N., Kaarianen, L., and Petterson, R.-F., 1983, Rubella virus contains one capsid protein and three envelope glycoproteins, El, E2a, and E2b, J. Virol. 46:964–973.PubMedGoogle Scholar
  129. Paabo, S., Bhat, B. M., Wold, W. S., and Peterson, P. A., 1987, A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum, Cell 50:311–317.PubMedCrossRefGoogle Scholar
  130. Palade, G., 1975, Intracellular aspects of the process of protein secretion, Science 89:347–358.CrossRefGoogle Scholar
  131. Pelham, H. R. B., 1988, Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment, EMBO J. 7:913–918.PubMedGoogle Scholar
  132. Pelham, H. R. B., 1989a, Control of protein exit from endoplasmic reticulum, Annu. Rev. Cell Biol. 5:1–23.PubMedCrossRefGoogle Scholar
  133. Pelham, H. R. B., 1989b, The selectivity of secretion: Protein sorting in the endoplasmic reticulum, Biochem. Soc. Trans. 17:795–802.PubMedGoogle Scholar
  134. Pelham, H. R. B., 1990, The retention signal for soluble proteins of the endoplasmic reticulum, Trends Biochem. Sci. 15:483–486.PubMedCrossRefGoogle Scholar
  135. Pelham, H. R. B., 1991, Recycling of proteins between the endoplasmic reticulum and the Golgi complex, Curr. Opin. Cell Biol. 3:585–591.PubMedCrossRefGoogle Scholar
  136. Pidoux, A. L., and Armstrong, J., 1992, Analysis of the BiP gene and identification of an ER retention signal in Schizosaccharomyces pombe, EMBO J. 11:1583–1591.PubMedGoogle Scholar
  137. Pihlajaniemi, T., Helaakoski, T., Tasanen, K., Myllyla, R., Huhtala, M. L., Koivu, J., and Kivirik-ko, K. I., 1987, Molecular cloning of the beta-subunit of human prolyl 4-hydroxylase: This subunit and protein disulphide isomerase are products of the same gene, EMBO J. 6:643–649.PubMedGoogle Scholar
  138. Plutner, H., Cox, A. D., Pind, S., Khosravi, F. R., Bourne, J. R., Schwaninger, R., Der, C. J., and Balch, W. E., 1991, Rablb regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments, J. Cell Biol. 115:31–43.PubMedCrossRefGoogle Scholar
  139. Plutner, H., Davidson, H., Saraste, J., and Balch, W., 1992, Morphological analysis of protein transport from the ER to Golgi membranes in Digitonin-permeablized cells: Role of p58-containing compartment, J. Cell Biol. 119:1097–1116.PubMedCrossRefGoogle Scholar
  140. Rose, J. K., and Bergmann, J. E., 1983, Altered cytoplasmic domains affect intracellular transport of the vesicular stomatitis virus glycoprotein, Cell 34:513–524.PubMedCrossRefGoogle Scholar
  141. Rose, J. K., and Doms, R. W., 1988, Regulation of protein export from the endoplasmic reticulum, Annu. Rev. Cell Biol. 4:257–288.PubMedCrossRefGoogle Scholar
  142. Rose, M. D., Misra, L. M., and Vogel, J. P., 1989, KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene, Cell 57:1211–1221.PubMedCrossRefGoogle Scholar
  143. Roth, J., 1987, Subcellular organization of glycosylation in mammalian cells, Biochim. Biophys. Acta 906:405–436.PubMedCrossRefGoogle Scholar
  144. Roth, M. G., and Compans, R. W., 1981, Delayed appearance of pseudotypes between vesicular stomatitis and influenza viruses during mixed infection of MDCK cells, J. Virol. 40:848–860.PubMedGoogle Scholar
  145. Rothman, J. E., 1987, Protein sorting by selective retention in the endoplasmic reticulum and Golgi stack, Cell 50:521–522.PubMedCrossRefGoogle Scholar
  146. Rottier, P. J. M., and Rose, J. K., 1987, Coronavirus El glycoprotein expressed from cloned cDNA localizes in the Golgi region, J. Virol. 61:2042–2045.PubMedGoogle Scholar
  147. Saraste, J., and Kuismanen, E., 1984, Pre-and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface, Cell 38:535–539.PubMedCrossRefGoogle Scholar
  148. Saraste, J., and 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.PubMedCrossRefGoogle Scholar
  149. Saraste, J., and Svensson, K., 1991, Distribution of the intermediate elements operating in ER to Golgi transport, J. Cell Sci. 100:415–430.PubMedGoogle Scholar
  150. Scheele, G., and Tartakoff, A., 1985, Exit of nonglycosylated secretory proteins from the rough endoplasmic reticulum is asynchronous in the exocrine pancreas, J. Biol. Chem. 260:926–931.PubMedGoogle Scholar
  151. Schekman, R., 1992, Genetic and biochemical analysis of vesicular traffic in yeast, Curr. Opin. Cell Biol. 4:587–592.PubMedCrossRefGoogle Scholar
  152. Schlegel, R., and Pardee, A. B., 1986, Caffeine-induced uncoupling of mitosis from the completion of DNA replication in mammalian cells, Science 232:1264–1266.PubMedCrossRefGoogle Scholar
  153. Schwaninger, R., Plutner, H., Bokoch, G., and Balch, W., 1992, Multiple GTP binding proteins regulate vesicular traffic from the ER to Golgi membranes, J. Cell Biol. 119:1077–1096.PubMedCrossRefGoogle Scholar
  154. Schweizer, A., Fransen, J. A. M., Baechi, T., Hauri, H. P., and Ginsel, G., 1988, Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus, J. Cell Biol. 107:1643–1653.PubMedCrossRefGoogle Scholar
  155. Schweizer, A., Matter, K., Ketcham, C. M., and Hauri, H. P., 1991, The isolated ER-Golgi intermediate compartment exhibits properties that are different from ER and cis-Golgi, J. Cell Biol. 113:45–54.PubMedCrossRefGoogle Scholar
  156. Schweizer, J., Fransen, J. A. M., Matter, K., Kries, T. E., Ginsel, G., and Hauri, H.-P., 1990, Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus, Eur. J. Cell Biol. 53:185–196.PubMedGoogle Scholar
  157. Sefton, B. M., and Buss, J. E., 1987, The covalent modification of eukaryotic proteins with lipid, J. Cell Biol 104:1449–1453.PubMedCrossRefGoogle Scholar
  158. Semenza, J. C., Hardwick, K. G., Dean, N., and Pelham, H. R., 1990, ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway, Cell 61:1349–1357.PubMedCrossRefGoogle Scholar
  159. Serafmi, T., Orci, L., Amherd, M., Brunner, M., Kahn, R., and Rothman, J., 1991, ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: A novel role for a GTP-binding protein, Cell 67:239–253.CrossRefGoogle Scholar
  160. Shim, J., Newman, A. P., and Ferro-Novick, S., 1991, The BOS1 gene encodes an essential 27-kD putative membrane protein that is required for vesicular transport from the ER to the Golgi complex in yeast, J. Cell Biol. 113:55–64.PubMedCrossRefGoogle Scholar
  161. Simons, K., and Fuller, S. D., 1985, Cell surface polarity in epithelia, Ann. Rev. Cell Biol. 1:243–288.PubMedCrossRefGoogle Scholar
  162. Simons, K., and Fuller, S. D., 1987, The budding of enveloped viruses: A paradigm for membrane sorting?, in Biological Organization: Molecular Interactions at High Resolution (R. M. Burnett and H. J. Vogel, eds.), pp. 139–150, Academic Press, New York.Google Scholar
  163. Simons, K., and van Meer, G., 1988, Lipid sorting in epithelial cells, J. Biochem. 27:6197–6202.CrossRefGoogle Scholar
  164. Sodeik, B., Doms, R. W., Ericsson, M., Hiller, G., Machamer, C. E., van’t Hof, W., van Meer, G., Moss, B., and Griffiths, G., 1993, Assembly of vaccinia virus: Role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks, J. Cell Biol. 121:521–541.PubMedCrossRefGoogle Scholar
  165. Spaan, W., Cavanagh, D., and Horzinek, M. C., 1988, Coronavirus: Structure and genome expression, J. Gen. Virol. 69:2939–2952.PubMedCrossRefGoogle Scholar
  166. Stirzaker, S. C., and Both, G. W., 1989, The signal peptide of the rotavirus glycoprotein VP7 is essential for its retention in the ER as an integral membrane protein, Cell 56:741–747.PubMedCrossRefGoogle Scholar
  167. Suzuki, C. K., Bonifacino, J. S., Lin, A. Y., Davis, M. M., and Klausner, R. D., 1991, Regulating the retention of T-cell receptor a chain variants within the endoplasmic reticulum: Ca2+-dependent association with BiP, J. Cell Biol. 114:189–205.PubMedCrossRefGoogle Scholar
  168. Sweet, D. J., and Pelham, H. R., 1992, The Saccharomyces cerevisiae SEC20 gene encodes a membrane glycoprotein which is sorted by the HDEL retrieval system, EMBO J. 11:423–432.PubMedGoogle Scholar
  169. Swift, A.M., and Machamer, C. E., 1991, A Golgi retention signal in a membrane-spanning domain of Coronavirus El protein, J. Cell Biol. 115:19–30.PubMedCrossRefGoogle Scholar
  170. Sztul, E., Kaplin, A., Saucan, L., and Palade, G., 1991, Protein traffic between distinct plasma membrane domains: Isolation and Characterization of vesicular carriers involved in transcytosis, Cell 64:81–89.PubMedCrossRefGoogle Scholar
  171. Takusuki, A., and Tamura, G., 1985, Brefeldin A, a specific inhibitor of intracellular translocation of vesicular stomatitis G protein: Intracellular accumulation of high mannose-type sugars and inhibition of its cell surface expression, Agric. Biol Chem. 45:899–902.CrossRefGoogle Scholar
  172. Tang, B. L., Wong, S. M., Qi, X. L., Low, S. H., and Hong, W., 1993, Molecular cloning characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor; J. Cell Biol. 120:325–328.PubMedCrossRefGoogle Scholar
  173. Terasaki, M., 1990, Recent progress on structural interactions of the endoplasmic reticulum, Cell Motil. 15:71–75.CrossRefGoogle Scholar
  174. Tilsdale, E., Bourne, J., Khosravi-Far, R., Der, C, and Balch, W., 1992, GTP binding mutants of rabl and rab2 are potent inhibitors of endoplasmic reticulum (ER) to Golgi transport, J. Cell Biol. 119:749–761.CrossRefGoogle Scholar
  175. Tooze, J., and Hollinshead, M., 1991, Tubular early endosomal networks in AtT20 and other cells, J. Cell Biol. 115:635–654.PubMedCrossRefGoogle Scholar
  176. Tooze, J., Kern, H. F., Fuller, S. D., and Howell, K. E., 1989, Condensation-sorting events in the rough endoplasmic reticulum of exocrine pancreatic cells, J. Cell Biol. 109:35–50.PubMedCrossRefGoogle Scholar
  177. Tooze, J., Tooze, S., and Warren, G., 1984, Replication of Coronavirus MHV-A59 in sac-cells: Determination of the first site of budding of progeny virions, Eur. J. Cell Biol. 33:281–293.PubMedGoogle Scholar
  178. Tooze, S. A., Tooze, J., and Warren, G., 1988, Site of addition of N-acetylgalactosamine to the El glycoprotein of mouse hepatitus virus-A59, J. Cell Biol. 106:1475–1487.PubMedCrossRefGoogle Scholar
  179. Tsao, Y. S., Ivessa, N. E., Adesnik, M., Sabatini, D. D., and Kreibich, G., 1992, Carboxy terminally truncated forms of ribophorin I are degraded in pre-Golgi compartments by a calcium-dependent process, J. Cell Biol. 116:57–67.PubMedCrossRefGoogle Scholar
  180. van Meer, G., 1989, Lipid traffic in animal cells, Annu. Rev. Cell Biol. 5:247–275.PubMedCrossRefGoogle Scholar
  181. Vaux, D., Tooze, J., and Fuller, S., 1990, Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal, Nature 345:495–502.PubMedCrossRefGoogle Scholar
  182. Vaux, D., Tooze, J., and Fuller, S., 1992, Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal (retraction), Nature 360:372.PubMedCrossRefGoogle Scholar
  183. von Bonsdorff, C., and Vaheri, A., 1969, Growth of rubella virus BHK21 cells: Electron microscopy of morphogenesis, J. Gen. Virol. 5:47–51.CrossRefGoogle Scholar
  184. Walter, P., and Blobel, G., 1982, Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum, Nature 299:691–698.PubMedCrossRefGoogle Scholar
  185. Walter, P., and Lingappa, V., 1986, Mechanisms of protein translocation across the endoplasmic reticulum membrane, Annu. Rev. Cell Biol. 2:499–516.PubMedCrossRefGoogle Scholar
  186. Wandinger-Ness, A., Bennett, M., Antony, C., and Simons, K., 1990, Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of epithelial cells, J. Cell Biol. 111:987–1000.PubMedCrossRefGoogle Scholar
  187. Warren, G., 1987, Signals and salvage sequences, Nature 327:17–18.PubMedCrossRefGoogle Scholar
  188. Weibel, E. R., Staübli, W., Gnägi, H. R., and Hess, F. A., 1969, Correlated morphometric and biochemical studies on the liver cell. I: Morphometric model, stereological methods and normal morphometric data for rat liver, J. Cell Biol. 42:68–91.PubMedCrossRefGoogle Scholar
  189. Wen, D., and Schlesinger, M. J., 1984, Fatty acid-acylated proteins in secretory mutants of Sac-charomyces cerevisiae, Mol. Cell Biol. 4:688–694.PubMedGoogle Scholar
  190. Wiedmann, M., Kurzchalia, T. V., Hartmann, E., and Rapoport, T. A., 1987, A signal sequence receptor in the endoplasmic reticulum membrane, Nature 328:830–833.PubMedCrossRefGoogle Scholar
  191. Wieland, F. T., Gleason, M. L., Serafini, T. A., and Rothman, J. E., 1987, The rate of bulk flow from the endoplasmic reticulum to the cell surface, Cell 50:289–300.PubMedCrossRefGoogle Scholar
  192. Wikstroem, L., and Lodish, H., 1991, Non-lysosomal pre-Golgi degredation of unassembled asialoglycoprotein receptor subunits: A TLCK-and TPCK-sensitive cleavage within the ER, J. Cell Biol. 113:997–1007.CrossRefGoogle Scholar
  193. Williams, D. B., Swiedler, S. J., and Hart, G. W., 1985, Intracellular transport of membrane glycoproteins: Two closely related histocompatibility antigens differ in their rates of transit to the cell surface, J. Cell Biol. 101:725–734.PubMedCrossRefGoogle Scholar
  194. Wilson, D. W., Wilcox, C. A., Flynn, G. C., Chen, E., Kuang, W.-J., Henzel, W. J., Block, M. R., Ullrich, A., and Rothman, J. E., 1989, A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast, Nature 339:355–359.PubMedCrossRefGoogle Scholar
  195. Yewdell, J. W., and Bennink, J. R., 1989, Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lyphocytes, Science 244:715–718.CrossRefGoogle Scholar
  196. Zagouras, P., and Rose, J. K., 1989, Carboxy-terminal SEKDEL sequences retard but do not retain two secretory proteins in the endoplasmic reticulum, J. Cell Biol. 109:2633–2640.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • Rob J. M. Hendriks
    • 1
  • Stephen D. Fuller
    • 2
  1. 1.Biological StructuresHeidelbergGermany
  2. 2.Biocomputing ProgrammeEuropean Molecular Biology LaboratoryHeidelbergGermany

Personalised recommendations