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ER to Golgi-Dependent Protein Secretion: The Conventional Pathway

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1459)

Abstract

Secretion is the cellular process present in every organism that delivers soluble proteins and cargoes to the extracellular space. In eukaryotes, conventional protein secretion (CPS) is the trafficking route that secretory proteins undertake when are transported from the endoplasmic reticulum (ER) to the Golgi apparatus (GA), and subsequently to the plasma membrane (PM) via secretory vesicles or secretory granules. This book chapter recalls the fundamental steps in cell biology research contributing to the elucidation of CPS; it describes the most prominent examples of conventionally secreted proteins in eukaryotic cells and the molecular mechanisms necessary to regulate each step of this process.

Key words

ER Ribosome SRP Translocon COPII COPI SNARE Golgi TGN Secretory vesicles Secretory granules Plasma membrane Regulated secretion 

References

  1. 1.
    Wooldridge K (2009) Bacterial secreted proteins: secretory mechanisms and role in pathogenesis. Caister Academic Press, Norfolk, VAGoogle Scholar
  2. 2.
    Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166. doi: 10.1016/S0092-8674(03)01079-1 PubMedCrossRefGoogle Scholar
  3. 3.
    Palade GE (1975) Intracellular aspects of the process of protein synthesis. Science 189:347–358. doi: 10.1126/science.1096303 PubMedCrossRefGoogle Scholar
  4. 4.
    Kelly RB (1985) Pathways of protein secretion in eukaryotes. Science 230:25–32. doi: 10.1126/science.2994224 PubMedCrossRefGoogle Scholar
  5. 5.
    Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243–293. doi: 10.1146/annurev.cb.03.110187.001331 PubMedCrossRefGoogle Scholar
  6. 6.
    Tooze SA, Martens GJ, Huttner WB (2001) Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol 11:116–122. doi: 10.1016/S0962-8924(00)01907-3 PubMedCrossRefGoogle Scholar
  7. 7.
    Porter KR, Claude A, Fullam EF (1945) A study of tissue culture cells by electron microscopy: methods and preliminary observations. J Exp Med 81:233–246. doi: 10.1084/jem.81.3.233 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Palade GE (1955) A small particulate component of the cytoplasm. J Biophys Biochem Cytol 1:59–68. doi: 10.1083/jcb.1.1.59 PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Palade GE (1955) Studies on the endoplasmic reticulum: II. Simple dispositions in cells in situ. J Biophys Biochem Cytol 1:567–582. doi: 10.1083/jcb.1.6.567 PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Palade GE, Siekevitz P (1956) Liver microsomes: an integrated morphological and biochemical study. J Biophys Biochem Cytol 2:171–200. doi: 10.1083/jcb.2.2.171 PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Palade GE, Siekevitz P (1956) Pancreatic microsomes: an integrated morphological and biochemical study. J Biophys Biochem Cytol 2:671–690. doi: 10.1083/jcb.2.6.671 PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Siekevitz P, Palade GE (1958) A cytochemical study on the pancreas of the guinea pig. I. Isolation and enzymatic activities of cell fractions. J Biophys Biochem Cytol 4:203–218. doi: 10.1083/jcb.4.2.203 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Siekevitz P, Palade GE (1958) A cytochemical study on the pancreas of the guinea pig. II. Functional variations in the enzymatic activity of microsomes. J Biophys Biochem Cytol 4:309–318. doi: 10.1083/jcb.4.3.309 PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Siekevitz P, Palade GE (1958) A cytochemical study on the pancreas of the guinea pig. III. In vivo incorporation of leucine-1-C14 into the proteins of cell fractions. J Biophys Biochem Cytol 4:557–566. doi: 10.1083/jcb.4.5.557 PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Siekevitz P, Palade GE (1960) A cytochemical study on the pancreas of the guinea pig. 5. In vivo incorporation of leucine-l-C 14 into the chymotrypsinogen of various cell fractions. J Biophys Biochem Cytol 7:619–630. doi: 10.1083/jcb.7.4.619 PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Redman CM, Siekevitz P, Palade GE (1966) Synthesis and transfer of amylase in pigeon pancreatic micromosomes. J Biol Chem 241:1150–1158PubMedGoogle Scholar
  17. 17.
    Redman CM, Sabatini DD (1966) Vectorial discharge of peptides released by puromycin from attached ribosomes. Proc Natl Acad Sci U S A 56:608–615. doi: 10.1073/pnas.56.2.608 PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Caro LG, Palade GE (1964) Protein synthesis, storage, and discharge in the pancreatic exocrine cell – an autoradiographic study. J Cell Biol 20:473–495. doi: 10.1083/jcb.20.3.473 PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Jamieson JD, Palade GE (1966) Role of the Golgi complex in the intracellular transport of secretory proteins. Proc Natl Acad Sci U S A 55:424–431. doi: 10.1073/pnas.55.2.424 PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Jamieson JD, Palade GE (1967) Intracellular transport of secretory proteins in pancreatic exocrine cell. I Role of peripheral elements of Golgi complex. J Cell Biol 34:577–596. doi: 10.1083/jcb.34.2.577 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Jamieson JD, Palade GE (1967) Intracellular transport of secretory proteins in the pancreatic exocrine cell. II Transport to condensing vacuoles and zymogen granules. J Cell Biol 34:597–615. doi: 10.1083/jcb.34.2.597 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Farquhar MG, Palade GE (1981) The Golgi apparatus (complex)-(1954–1981)-from artifact to center stage. J Cell Biol 91:77–103. doi: 10.1083/jcb.91.3.77s PubMedCentralCrossRefGoogle Scholar
  23. 23.
    Blobel G, Sabatini D (1971) Dissociation of mammalian polyribosomes into subunits by puromycin. In: Manson LA (ed) Biomembranes. Springer, Berlin, pp 193–195CrossRefGoogle Scholar
  24. 24.
    Swan D, Aviv H, Leder P (1972) Purification and properties of biologically active messenger RNA for a myeloma light chain. Proc Natl Acad Sci U S A 69:1967–1971. doi: 10.1073/pnas.69.7.1967 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Milstein C, Brownlee GG, Harrison TM, Mathews MB (1972) A possible precursor of immunoglobulin light chains. Nat New Biol 239:117–120. doi: 10.1038/newbio239117a0 PubMedCrossRefGoogle Scholar
  26. 26.
    Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. I Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67:835–851. doi: 10.1083/jcb.67.3.835 PubMedCrossRefGoogle Scholar
  27. 27.
    Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. II Reconstitution of functional rough microsomes from heterologous components. J Cell Biol 67:852–862. doi: 10.1083/jcb.67.3.852 PubMedCrossRefGoogle Scholar
  28. 28.
    Warren G, Dobberstein B (1978) Protein transfer across microsomal membranes reassembled from separated membrane components. Nature 273:569–571. doi: 10.1038/273569a0 PubMedCrossRefGoogle Scholar
  29. 29.
    Walter P, Blobel G (1980) Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum. Proc Natl Acad Sci U S A 77:7112–7116. doi: 10.1073/pnas.77.12.7112 PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Walter P, Ibrahimi I, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol 91:545–550. doi: 10.1083/jcb.91.2.545 PubMedCrossRefGoogle Scholar
  31. 31.
    Walter P, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J Cell Biol 91:551–556. doi: 10.1083/jcb.91.2.551 PubMedCrossRefGoogle Scholar
  32. 32.
    Walter P, Blobel G (1981) Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J Cell Biol 91:557–561. doi: 10.1083/jcb.91.2.557 PubMedCrossRefGoogle Scholar
  33. 33.
    Gilmore R, Blobel G (1983) Transient involvement of signal recognition particle and its receptor in the microsomal membrane prior to protein translocation. Cell 35:677–685. doi: 10.1016/0092-8674(83)90100-9 PubMedCrossRefGoogle Scholar
  34. 34.
    Kurzchalia TV, Wiedmann M, Girshovich AS, Bochkareva ES, Bielka H, Rapoport TA (1986) The signal sequence of nascent preprolactin interacts with the 54K polypeptide of the signal recognition particle. Nature 320:634–636. doi: 10.1038/320634a0 PubMedCrossRefGoogle Scholar
  35. 35.
    Krieg UC, Walter P, Johnson AE (1986) Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc Natl Acad Sci U S A 83:8604–8608. doi: 10.1073/pnas.83.22.8604 PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Siegel V, Walter P (1988) Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP. Cell 52:39–49. doi: 10.1016/0092-8674(88)90529-6 PubMedCrossRefGoogle Scholar
  37. 37.
    Bernstein HD, Poritz MA, Strub K, Hoben PJ, Brenner S, Walter P (1989) Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature 340:482–486. doi: 10.1038/340482a0 PubMedCrossRefGoogle Scholar
  38. 38.
    Walter P, Blobel G (1982) Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature 299:691–698. doi: 10.1038/299691a0 PubMedCrossRefGoogle Scholar
  39. 39.
    Meyer DI, Dobberstein B (1980) 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. doi: 10.1083/jcb.87.2.498 PubMedCrossRefGoogle Scholar
  40. 40.
    Meyer DI, Dobberstein B (1980) 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. doi: 10.1083/jcb.87.2.503 PubMedCrossRefGoogle Scholar
  41. 41.
    Meyer DI, Louvard D, Dobberstein B (1982) Characterization of molecules involved in protein translocation using a specific antibody. J Cell Biol 92:579–583. doi: 10.1083/jcb.92.2.579 PubMedCrossRefGoogle Scholar
  42. 42.
    Meyer DI, Krause E, Dobberstein B (1982) Secretory protein translocation across membranes-the role of the “docking protein”. Nature 297:647–650. doi: 10.1038/297647a0 PubMedCrossRefGoogle Scholar
  43. 43.
    Gilmore R, Blobel G, Walter P (1982) Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J Cell Biol 95:463–469. doi: 10.1083/jcb.95.2.463 PubMedCrossRefGoogle Scholar
  44. 44.
    Gilmore R, Walter P, Blobel G (1982) Protein translocation across the endoplasmic reticulum. II. Isolation and characterization of the signal recognition particle receptor. J Cell Biol 95:470–477. doi: 10.1083/jcb.95.2.470 PubMedCrossRefGoogle Scholar
  45. 45.
    Tajima S, Lauffer L, Rath VL, Walter P (1986) The signal recognition particle receptor is a complex that contains two distinct polypeptide chains. J Cell Biol 103:1167c1178. doi: 10.1083/jcb.103.4.1167
  46. 46.
    Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Annu Rev Biochem 70:755–775. doi: 10.1146/annurev.biochem.70.1.755 PubMedCrossRefGoogle Scholar
  47. 47.
    Römisch K, Webb J, Herz J, Prehn S, Frank R, Vingron M, Dobberstein B (1989) Homology of 54K protein of signal-recognition particle, docking protein and two E. coli proteins with putative GTP-binding domains. Nature 340:478–482. doi: 10.1038/340478a0 PubMedCrossRefGoogle Scholar
  48. 48.
    Poritz MA, Bernstein HD, Strub K, Zopf D, Wilhelm H, Walter P (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250:1111–1117. doi: 10.1126/science.1701272 PubMedCrossRefGoogle Scholar
  49. 49.
    Wolin SL (1994) From the elephant to E. coli: SRP-dependent protein targeting. Cell 77:787–790PubMedCrossRefGoogle Scholar
  50. 50.
    Connolly T, Gilmore R (1986) Formation of a functional ribosome-membrane junction during translocation requires the participation of a GTP-binding protein. J Cell Biol 103:2253–2261. doi: 10.1083/jcb.103.6.2253 PubMedCrossRefGoogle Scholar
  51. 51.
    Connolly T, Gilmore R (1989) The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell 57:599–610. doi: 10.1016/0092-8674(89)90129-3 PubMedCrossRefGoogle Scholar
  52. 52.
    Connolly T, Rapiejko PJ, Gilmore R (1991) Requirement of GTP hydrolysis for dissociation of the signal recognition particle from its receptor. Science 252:1171–1173. doi: 10.1126/science.252.5009.1171 PubMedCrossRefGoogle Scholar
  53. 53.
    Walter P, Lingappa VR (1986) Mechanism of protein translocation across the endoplasmic reticulum membrane. Annu Rev Cell Biol 2:499–516. doi: 10.1146/annurev.cb.02.110186.002435 PubMedCrossRefGoogle Scholar
  54. 54.
    Simon SM, Blobel G, Zimmerberg J (1989) Large aqueous channels in membrane vesicles derived from the rough endoplasmic reticulum of canine pancreas or the plasma membrane of Escherichia coli. Proc Natl Acad Sci U S A 86:6176–6180. doi: 10.1073/pnas.86.16.6176 PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Simon SM, Blobel G (1991) A protein-conducting channel in the endoplasmic reticulum. Cell 65:371–380. doi: 10.1016/0092-8674(91)90455-8 PubMedCrossRefGoogle Scholar
  56. 56.
    Krieg UC, Johnson AE, Walter P (1989) Protein translocation across the endoplasmic reticulum membrane: identification by photocross-linking of a 39-kDa integral membrane glycoprotein as part of a putative translocation tunnel. J Cell Biol 109:2033–2043. doi: 10.1083/jcb.109.5.2033 PubMedCrossRefGoogle Scholar
  57. 57.
    Wiedmann M, Görlich D, Hartmann E, Kurzchalia TV, Rapoport TA (1989) Photocrosslinking demonstrates proximity of a 34 kDa membrane protein to different portions of preprolactin during translocation through the endoplasmic reticulum. FEBS Lett 257:263–268. doi: 10.1016/0014-5793(89)81549-2 PubMedCrossRefGoogle Scholar
  58. 58.
    High S, Görlich D, Wiedmann M, Rapoport TA, Dobberstein B (1991) The identification of proteins in the proximity of signal-anchor sequences during their targeting to and insertion into the membrane of the ER. J Cell Biol 113:35–44. doi: 10.1083/jcb.113.1.35 PubMedCrossRefGoogle Scholar
  59. 59.
    Thrift RN, Andrews DW, Walter P, Johnson AE (1991) A nascent membrane protein is located adjacent to ER membrane proteins throughout its integration and translation. J Cell Biol 112:809–821. doi: 10.1083/jcb.112.5.809 PubMedCrossRefGoogle Scholar
  60. 60.
    Nicchitta CV, Blobel G (1990) Assembly of translocation-competent proteoliposomes from detergent-solubilized rough microsomes. Cell 60:259–269. doi: 10.1016/0092-8674(90)90741-V PubMedCrossRefGoogle Scholar
  61. 61.
    Görlich D, Hartmann E, Prehn S, Rapoport TA (1992) A protein of the endoplasmic reticulum involved early in polypeptide translocation. Nature 357:47–52. doi: 10.1038/357047a0 PubMedCrossRefGoogle Scholar
  62. 62.
    Görlich D, Prehn S, Hartmann E, Kalies KU, Rapoport TA (1992) A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell 71:489–503. doi: 10.1016/0092-8674(92)90517-G PubMedCrossRefGoogle Scholar
  63. 63.
    Görlich D, Rapoport TA (1993) Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75:615–630. doi: 10.1016/0092-8674(93)90483-7 PubMedCrossRefGoogle Scholar
  64. 64.
    Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:205–215. doi: 10.1016/0092-8674(80)90128-2 PubMedCrossRefGoogle Scholar
  65. 65.
    Deshaies RJ, Schekman R (1987) A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J Cell Biol 105:633–645. doi: 10.1083/jcb.105.2.633 PubMedCrossRefGoogle Scholar
  66. 66.
    Hartmann E, Sommer T, Prehn S, Görlich D, Jentsch S, Rapoport TA (1994) Evolutionary conservation of components of the protein translocation complex. Nature 367:654–657. doi: 10.1038/367654a0 PubMedCrossRefGoogle Scholar
  67. 67.
    Brundage L, Hendrick JP, Schiebel E, Driessen AJ, Wickner W (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62:649–657. doi: 10.1016/0092-8674(90)90111-Q PubMedCrossRefGoogle Scholar
  68. 68.
    Akimaru J, Matsuyama S, Tokuda H, Mizushima S (1991) Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli. Proc Natl Acad Sci U S A 88:6545–6549. doi: 10.1073/pnas.88.15.6545 PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Hartmann E, Görlich D, Kostka S, Otto A, Kraft R, Knespel S, Bürger E, Rapoport TA, Prehn S (1993) A tetrameric complex of membrane proteins in the endoplasmic reticulum. Eur J Biochem 214:375–381. doi: 10.1111/j.1432-1033.1993.tb17933.x PubMedCrossRefGoogle Scholar
  70. 70.
    Kelleher DJ, Kreibich G, Gilmore R (1992) Oligosaccharyltransferase activity is associated with a protein complex composed of ribophorins I and II and a 48 kd protein. Cell 69:55–65. doi: 10.1016/0092-8674(92)90118-V PubMedCrossRefGoogle Scholar
  71. 71.
    Kelleher DJ, Gilmore R (1997) DAD1, the defender against apoptotic cell death, is a subunit of the mammalian oligosaccharyltransferase. Proc Natl Acad Sci U S A 94:4994–4999. doi: 10.1073/pnas.94.10.4994 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Nilsson I, Kelleher DJ, Miao Y, Shao Y, Kreibich G, Gilmore R, von Heijne G, Johnson AE (2003) Photocross-linking of nascent chains to the STT3 subunit of the oligosaccharyltransferase complex. J Cell Biol 161:715–725. doi: 10.1083/jcb.200301043 PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Evans EA, Gilmore R, Blobel G (1986) Purification of microsomal signal peptidase as a complex. Proc Natl Acad Sci U S A 83:581–585. doi: 10.1073/pnas.83.3.581 PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Meyer HA, Grau H, Kraft R, Kostka S, Prehn S, Kalies KU, Hartmann E (2000) Mammalian Sec61 is associated with Sec62 and Sec63. J Biol Chem 275:14550–14557. doi: 10.1074/jbc.275.19.14550 PubMedCrossRefGoogle Scholar
  75. 75.
    Tyedmers J, Lerner M, Bies C, Dudek J, Skowronek MH, Haas IG, Heim N, Nastainczyk W, Volkmer J, Zimmermann R (2000) Homologs of the yeast Sec complex subunits Sec62p and Sec63p are abundant proteins in dog pancreas microsomes. Proc Natl Acad Sci U S A 97:7214–7219. doi: 10.1073/pnas.97.13.7214 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Böhni PC, Deshaies RJ, Schekman RW (1988) SEC11 is required for signal peptide processing and yeast cell growth. J Cell Biol 106:1035–1042. doi: 10.1083/jcb.106.4.1035 PubMedCrossRefGoogle Scholar
  77. 77.
    Dempski RE Jr, Imperiali B (2002) Oligosaccharyl transferase: gatekeeper to the secretory pathway. Curr Opin Chem Biol 6:844–850. doi: 10.1016/S1367-5931(02)00390-3 PubMedCrossRefGoogle Scholar
  78. 78.
    Mothes W, Heinrich SU, Graf R, Nilsson I, von Heijne G, Brunner J, Rapoport TA (1997) Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 89:523–533. doi: 10.1016/S0092-8674(00)80234-2 PubMedCrossRefGoogle Scholar
  79. 79.
    Ng DT, Brown JD, Walter P (1996) Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J Cell Biol 134:269–278. doi: 10.1083/jcb.134.2.269 PubMedCrossRefGoogle Scholar
  80. 80.
    Hansen W, Garcia PD, Walter P (1986) In vitro protein translocation across the yeast endoplasmic reticulum: ATP-dependent posttranslational translocation of the prepro-alpha-factor. Cell 45:397–406. doi: 10.1016/0092-8674(86)90325-9 PubMedCrossRefGoogle Scholar
  81. 81.
    Chirico WJ, Waters MG, Blobel G (1988) 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332:805–810. doi: 10.1038/332805a0 PubMedCrossRefGoogle Scholar
  82. 82.
    Deshaies RJ, Sanders SL, Feldheim DA, Schekman R (1991) Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349:806–808. doi: 10.1038/349806a0 PubMedCrossRefGoogle Scholar
  83. 83.
    Panzner S, Dreier L, Hartmann E, Kostka S, Rapoport TA (1995) Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81:561–570. doi: 10.1016/0092-8674(95)90077-2 PubMedCrossRefGoogle Scholar
  84. 84.
    Hanein D, Matlack KES, Jungnickel B, Plath K, Kalies KU, Miller KR, Rapoport TA, Akey CW (1996) Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 87:721–732. doi: 10.1016/S0092-8674(00)81391-4 PubMedCrossRefGoogle Scholar
  85. 85.
    Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450:663–669. doi: 10.1038/nature06384 PubMedCrossRefGoogle Scholar
  86. 86.
    Johnson N, Powis K, High S (2013) Post-translational translocation into the endoplasmic reticulum. Biochim Biophys Acta 1833:2403–2409. doi: 10.1016/j.bbamcr.2012.12.008 PubMedCrossRefGoogle Scholar
  87. 87.
    Stefanovic S, Hegde RS (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128:1147–1159. doi: 10.1016/j.cell.2007.01.036 PubMedCrossRefGoogle Scholar
  88. 88.
    Favaloro V, Spasic M, Schwappach B, Dobberstein B (2008) Distinct targeting pathways for the membrane insertion of tail-anchored (TA) proteins. J Cell Sci 121:1832–1840. doi: 10.1242/jcs.020321 PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Mariappan M, Li X, Stefanovic S, Sharma A, Mateja A, Keenan RJ, Hegde RS (2010) A ribosome-associating factor chaperones tail-anchored membrane proteins. Nature 466:1120–1124. doi: 10.1038/nature09296 PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Schuldiner M, Metz J, Schmid V, Denic V, Rakwalska M, Schmitt HD, Schwappach B, Weissman JS (2008) The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134:634–645. doi: 10.1016/j.cell.2008.06.025 PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Vilardi F, Lorenz H, Dobberstein B (2011) WRB is the receptor for TRC40/Asna1-mediated insertion of tail-anchored proteins into the ER membrane. J Cell Sci 124:1301–1307. doi: 10.1242/jcs.084277 PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Yamamoto Y, Sakisaka T (2012) Molecular machinery for insertion of tail-anchored membrane proteins into the endoplasmic reticulum membrane in mammalian cells. Mol Cell 48:387–397. doi: 10.1016/j.molcel.2012.08.028 PubMedCrossRefGoogle Scholar
  93. 93.
    Mariappan M, Mateja A, Dobosz M, Bove E, Hegde RS, Keenan RJ (2011) The mechanism of membrane-associated steps in tail-anchored protein insertion. Nature 477:61–66. doi: 10.1038/nature10362 PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–1086. doi: 10.1126/science.1209038 PubMedCrossRefGoogle Scholar
  95. 95.
    Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499. doi: 10.1146/annurev-arplant-050312-120053 PubMedCrossRefGoogle Scholar
  96. 96.
    Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzola M, Amherdt M, Schekman R (1994) COPII–a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895–907. doi: 10.1016/0092-8674(94)90138-4 PubMedCrossRefGoogle Scholar
  97. 97.
    Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14:382–392. doi: 10.1038/nrm3588 PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Nakano A, Muramatsu M (1989) A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J Cell Biol 109:2677–2691. doi: 10.1083/jcb.109.6.2677 PubMedCrossRefGoogle Scholar
  99. 99.
    Yoshihisa T, Barlowe C, Schekman R (1993) Requirement for a GTPase-activating protein in vesicle budding from the endoplasmic reticulum. Science 259:1466–1468. doi: 10.1126/science.8451644 PubMedCrossRefGoogle Scholar
  100. 100.
    Nakano A, Brada D, Schekman R (1988) A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J Cell Biol 107:851–863. doi: 10.1083/jcb.107.3.851 PubMedCrossRefGoogle Scholar
  101. 101.
    Barlowe C, Schekman R (1993) SEC12 encodes a guanine-nucleotide- exchange factor essential for transport vesicle budding from the ER. Nature 365:347–349. doi: 10.1038/365347a0 PubMedCrossRefGoogle Scholar
  102. 102.
    Goldberg J (1998) Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 95:237–248. doi: 10.1016/S0092-8674(00)81754-7 PubMedCrossRefGoogle Scholar
  103. 103.
    Huang M, Weissman JT, Beraud-Dufour S, Luan P, Wang C, Chen W, Aridor M, Wilson IA, Balch WE (2001) Crystal structure of Sar1-GDP at 1.7 Å resolution and the role of the NH2 terminus in ER export. J Cell Biol 155:937–948. doi: 10.1083/jcb.200106039 PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Lee MC, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R (2005) Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122:605–617. doi: 10.1016/j.cell.2005.07.025 PubMedCrossRefGoogle Scholar
  105. 105.
    Matsuoka K, Orci L, Amherdt M, Bednarek SY, Hamamoto S, Schekman R, Yeung T (1998) COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93:263–275. doi: 10.1016/S0092-8674(00)81577-9 PubMedCrossRefGoogle Scholar
  106. 106.
    Bi X, Corpina RA, Goldberg J (2002) Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419:271–277. doi: 10.1038/nature01040 PubMedCrossRefGoogle Scholar
  107. 107.
    Stagg SM, Gürkan C, Fowler DM, LaPointe P, Foss TR, Potter CS, Carragher B, Balch WE (2006) Structure of the Sec13/31 COPII coat cage. Nature 439:234–238. doi: 10.1038/nature04339 PubMedCrossRefGoogle Scholar
  108. 108.
    Fath S, Mancias JD, Bi X, Goldberg J (2007) Structure and organization of coat proteins in the COPII cage. Cell 129:1325–1336. doi: 10.1016/j.cell.2007.05.036 PubMedCrossRefGoogle Scholar
  109. 109.
    Stagg SM, LaPointe P, Razvi A, Gürkan C, Potter CS, Carragher B, Balch WE (2008) Structural basis for cargo regulation of COPII coat assembly. Cell 134:474–484. doi: 10.1016/j.cell.2008.06.024 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S, Orci L, Schekman R (2003) Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:497–509. doi: 10.1016/S0092-8674(03)00609-3 PubMedCrossRefGoogle Scholar
  111. 111.
    Sato K, Nakano A (2005) Dissection of COPII subunit-cargo assembly and disassembly kinetics during Sar1p-GTP hydrolysis. Nat Struct Mol Biol 12:167–174. doi: 10.1038/nsmb893 PubMedCrossRefGoogle Scholar
  112. 112.
    Bi X, Mancias JD, Goldberg J (2007) Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev Cell 13:635–645. doi: 10.1016/j.devcel.2007.10.006 PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Watson P, Townley AK, Koka P, Palmer KJ, Stephens DJ (2006) Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic 7:1678–1687. doi: 10.1111/j.1600-0854.2006.00493.x PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Connerly PL, Esaki M, Montegna EA, Strongin DE, Levi S, Soderholm J, Glick BS (2005) Sec16 is a determinant of transitional ER organization. Curr Biol 15:1439–1447. doi: 10.1016/j.cub.2005.06.065 PubMedCrossRefGoogle Scholar
  115. 115.
    Hughes H, Budnik A, Schmidt K, Palmer KJ, Mantell J, Noakes C, Johnson A, Carter DA, Verkade P, Watson P, Stephens DJ (2009) Organisation of human ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J Cell Sci 122:2924–2934. doi: 10.1242/jcs.044032 PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Whittle JR, Schwartz TU (2010) Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol 190:347–361. doi: 10.1083/jcb.201003092 PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R (2011) COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14:20–28. doi: 10.1038/ncb2390 PubMedCrossRefGoogle Scholar
  118. 118.
    O’Kelly I, Butler MH, Zilberberg N, Goldstein SA (2002) Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111:577–588. doi: 10.1016/S0092-8674(02)01040-1 PubMedCrossRefGoogle Scholar
  119. 119.
    Nakamura T, Hayashi T, Nasu-Nishimura Y, Sakaue F, Morishita Y, Okabe T, Ohwada S, Matsuura K, Akiyama T (2008) PX-RICS mediates ER-to-Golgi transport of the N-cadherin/beta-catenin complex. Genes Dev 22:1244–1256. doi: 10.1101/gad.1632308 PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Wang J, Hamblet NS, Mark S, Dickinson ME, Brinkman BC, Segil N, Fraser SE, Chen P, Wallingford JB, Wynshaw-Boris A (2006) Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133:1767–1778. doi: 10.1242/dev.02347 PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, Shao Y, Lee HJ, Wu AL, Fang Y, Satlin LM, Dow JT, Chen J, Zheng J, Boutros M, Mlodzik M (2009) Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat Cell Biol 11:286–294. doi: 10.1038/ncb1836 PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Malhotra V, Erlmann P (2015) The pathway of collagen secretion. Annu Rev Cell Dev Biol. doi: 10.1146/annurev-cellbio-100913-013002 PubMedGoogle Scholar
  123. 123.
    Townley AK, Feng Y, Schmidt K, Carter DA, Porter R, Verkade P, Stephens DJ (2008) Efficient coupling of Sec23–Sec24 to Sec13–Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J Cell Sci 121:3025–3034. doi: 10.1242/jcs.031070 PubMedCrossRefGoogle Scholar
  124. 124.
    Sarmah S, Barrallo-Gimeno A, Melville DB, Topczewski J, Solnica-Krezel L, Knapik EW (2010) Sec24D dependent transport of extracellular matrix proteins is required for zebrafish skeletal morphogenesis. PLoS One 5, e10367. doi: 10.1371/journal.pone.0010367 PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Boyadjiev SA, Kim SD, Hata A, Haldeman-Englert C, Zackai EH, Naydenov C, Hamamoto S, Schekman RW, Kim J (2011) Cranio-lenticulo-sutural dysplasia associated with defects in collagen secretion. Clin Genet 80:169–176. doi: 10.1111/j.1399-0004.2010.01550.x PubMedCrossRefGoogle Scholar
  126. 126.
    Venditti R, Scanu T, Santoro M, Di Tullio G, Spaar A, Gaibisso R, Beznoussenko GV, Mironov AA, Mironov A Jr, Zelante L, Piemontese MR, Notarangelo A, Malhotra V, Vertel BM, Wilson C, De Matteis MA (2012) Sedlin controls the ER export of procollagen by regulating the Sar1 cycle. Science 337:1668–1672. doi: 10.1126/science.1224947 PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Nogueira C, Erlmann P, Villeneuve J, Santos AJ, Martínez-Alonso E, Martínez-Menárguez JÁ, Malhotra V (2014) SLY1 and Syntaxin 18 specify a distinct pathway for procollagen VII export from the endoplasmic reticulum. Elife 3, e02784. doi: 10.7554/eLife.02784 PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Bacia K, Futai E, Prinz S, Meister A, Daum S, Glatte D, Briggs JA, Schekman R (2011) Multibudded tubules formed by COPII on artificial liposomes. Sci Rep 1:17. doi: 10.1038/srep00017 PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Zanetti G, Prinz S, Daum S, Meister A, Schekman R, Bacia K, Briggs JA (2013) The structure of the COPII transport-vesicle coat assembled on membranes. Elife 2, e00951. doi: 10.7554/eLife.00951 PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, Kitayama H, Guizzunti G, Hu Y, Wendler F, Dasgupta R, Perrimon N, Malhotra V (2006) Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439:604–607. doi: 10.1038/nature04377 PubMedCrossRefGoogle Scholar
  131. 131.
    Lerner DW, McCoy D, Isabella AJ, Mahowald AP, Gerlach GF, Chaudhry TA, Horne-Badovinac S (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24:159–168. doi: 10.1016/j.devcel.2012.12.005 PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Saito K, Chen M, Bard F, Chen S, Zhou H, Woodley D, Polischuk R, Schekman R, Malhotra V (2009) TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136:891–902. doi: 10.1016/j.cell.2008.12.025 PubMedCrossRefGoogle Scholar
  133. 133.
    Saito K, Yamashiro K, Ichikawa Y, Erlmann P, Kontani K, Malhotra V, Katada T (2011) cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites. Mol Biol Cell 22:2301–2308. doi: 10.1091/mbc.E11-02-0143 PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Saito K, Yamashiro K, Shimazu N, Tanabe T, Kontani K, Katada T (2014) Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export. J Cell Biol 206:751–762. doi: 10.1083/jcb.201312062 PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Wieland FT, Gleason ML, Serafini TA, Rothman JE (1987) The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell 50:289–300. doi: 10.1016/0092-8674(87)90224-8 PubMedCrossRefGoogle Scholar
  136. 136.
    Denecke J, Botterman J, Deblaere R (1990) Protein secretion in plant cells can occur via a default pathway. Plant Cell 2:51–59. doi: 10.1105/tpc.2.1.51 PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Phillipson BA, Pimpl P, daSilva LL, Crofts AJ, Taylor JP, Movafeghi A, Robinson DG, Denecke J (2001) Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell 13:2005–2020. doi:10.1105/TPC.010110Google Scholar
  138. 138.
    Thor F, Gautschi M, Geiger R, Helenius A (2009) Bulk flow revisited: transport of a soluble protein in the secretory pathway. Traffic 10:1819–1830. doi: 10.1111/j.1600-0854.2009.00989.x PubMedCrossRefGoogle Scholar
  139. 139.
    Kappeler F, Klopfenstein DR, Foguet M, Paccaud JP, Hauri HP (1997) The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII. J Biol Chem 272:31801–31808. doi: 10.1074/jbc.272.50.31801 PubMedCrossRefGoogle Scholar
  140. 140.
    Nishimura N, Balch WE (1997) A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277:556–558. doi: 10.1126/science.277.5325.556 PubMedCrossRefGoogle Scholar
  141. 141.
    Contreras I, Yang Y, Robinson DG, Aniento F (2004) Sorting signals in the cytosolic tail of plant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol 45:1779–1786. doi: 10.1093/pcp/pch200 PubMedCrossRefGoogle Scholar
  142. 142.
    Hanton SL, Renna L, Bortolotti LE, Chatre L, Stefano G, Brandizzi F (2005) Diacidic motifs influence the export of transmembrane proteins from the endoplasmic reticulum in plant cells. Plant Cell 17:3081–3093. doi: 10.1105/tpc.105.034900 PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Hay JC, Chao DS, Kuo CS, Scheller RH (1997) Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell 89:149–158. doi: 10.1016/S0092-8674(00)80191-9 PubMedCrossRefGoogle Scholar
  144. 144.
    Cao X, Ballew N, Barlowe C (1998) Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J 17:2156–2165. doi: 10.1093/emboj/17.8.2156 PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Allan BB, Moyer BD, Balch WE (2000) Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 289:444–448. doi: 10.1126/science.289.5478.444 PubMedCrossRefGoogle Scholar
  146. 146.
    Moyer BD, Allan BB, Balch WE (2001) Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2:268–276. doi: 10.1034/j.1600-0854.2001.1o007.x PubMedCrossRefGoogle Scholar
  147. 147.
    Sacher M, Barrowman J, Wang W, Horecka J, Zhang Y, Pypaert M, Ferro-Novick S (2001) TRAPP I implicated in the specificity of tethering in ER-to-Golgi transport. Mol Cell 7:433–442. doi: 10.1016/S1097-2765(01)00190-3 PubMedCrossRefGoogle Scholar
  148. 148.
    Shorter J, Beard MB, Seemann J, Dirac-Svejstrup AB, Warren G (2002) Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115. J Cell Biol 157:45–62. doi: 10.1083/jcb.200112127 PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Cai Y, Chin HF, Lazarova D, Menon S, Fu C, Cai H, Sclafani A, Rodgers DW, De La Cruz EM, Ferro-Novick S, Reinisch KM (2008) The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133:1202–1213. doi: 10.1016/j.cell.2008.04.049 PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Wong M, Munro S (2014) Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science 346:1256898. doi: 10.1126/science.1256898
  151. 151.
    Cai H, Yu S, Menon S, Cai Y, Lazarova D, Fu C, Reinisch K, Hay JC, Ferro-Novick S (2007) TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445:941–944. doi: 10.1038/nature05527 PubMedCrossRefGoogle Scholar
  152. 152.
    Lord C, Bhandari D, Menon S, Ghassemian M, Nycz D, Hay J, Ghosh P, Ferro-Novick S (2011) Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473:181–186. doi: 10.1038/nature09969 PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Rowe T, Dascher C, Bannykh S, Plutner H, Balch WE (1998) Role of vesicle-associated syntaxin 5 in the assembly of pre-Golgi intermediates. Science 279:696–700. doi: 10.1126/science.279.5351.696 PubMedCrossRefGoogle Scholar
  154. 154.
    Xu D, Joglekar AP, Williams AL, Hay JC (2000) Subunit structure of a mammalian ER/Golgi SNARE complex. J Biol Chem 275:39631–39639. doi: 10.1074/jbc.M007684200 PubMedCrossRefGoogle Scholar
  155. 155.
    Lowe SL, Peter F, Subramaniam VN, Wong SH, Hong W (1997) A SNARE involved in protein transport through the Golgi apparatus. Nature 389:881–884. doi: 10.1038/39923 PubMedCrossRefGoogle Scholar
  156. 156.
    Yamaguchi T, Dulubova I, Min SW, Chen X, Rizo J, Südhof TC (2002) Sly1 binds to Golgi and ER syntaxins via a conserved N-terminal peptide motif. Dev Cell 2:295–305. doi: 10.1016/S1534-5807(02)00125-9 PubMedCrossRefGoogle Scholar
  157. 157.
    Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324. doi: 10.1038/362318a0 PubMedCrossRefGoogle Scholar
  158. 158.
    Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395:347–353. doi: 10.1038/26412 PubMedCrossRefGoogle Scholar
  159. 159.
    Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Söllner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772. doi: 10.1016/S0092-8674(00)81404-X PubMedCrossRefGoogle Scholar
  160. 160.
    Parlati F, McNew JA, Fukuda R, Miller R, Söllner TH, Rothman JE (2000) Topological restriction of SNARE-dependent membrane fusion. Nature 407:194–198. doi: 10.1038/35025076 PubMedCrossRefGoogle Scholar
  161. 161.
    Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–477. doi: 10.1126/science.1161748 PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA. (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1142. doi:10.1104/pp.121.4.1127Google Scholar
  163. 163.
    Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447. doi: 10.1046/j.1365-313X.1998.00208.x PubMedCrossRefGoogle Scholar
  164. 164.
    Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146:1098–1108. doi: 10.1104/pp.107.113647 PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109–1116. doi: 10.1104/pp.107.113654 PubMedPubMedCentralCrossRefGoogle Scholar
  166. 166.
    Prokhnevsky AI, Peremyslov VV, Dolja VV (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A 105:19744–19749. doi: 10.1073/pnas.0810730105 PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot 59:2499–2512. doi: 10.1093/jxb/ern114 PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Sparkes IA, Ketelaar T, Ruijter NC, Hawes C (2009) Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic 10:567–571. doi: 10.1111/j.1600-0854.2009.00891.x PubMedCrossRefGoogle Scholar
  169. 169.
    Brandizzi F, Snapp EL, Roberts AG, Lippincott-Schwartz J, Hawes C (2002) Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14:1293–1309. doi:10.1105/tpc.001586Google Scholar
  170. 170.
    Kang BH, Staehelin LA (2008) ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma 234:51–64. doi: 10.1007/s00709-008-0015-6 PubMedCrossRefGoogle Scholar
  171. 171.
    daSilva LLP, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F (2004) Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16, 1753–1771. doi:10.1105/tpc.022673Google Scholar
  172. 172.
    Stefano G, Renna L, Chatre L, Hanton SL, Moreau P, Hawes C, Brandizzi F (2006) In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J 46:95–110. doi: 10.1111/j.1365-313X.2006.02675.x PubMedCrossRefGoogle Scholar
  173. 173.
    Langhans M, Meckel T, Kress A, Lerich A, Robinson DG (2012) ERES (ER exit sites) and the “secretory unit concept”. J Microsc 247:48–59. doi: 10.1111/j.1365-2818.2011.03597.x PubMedCrossRefGoogle Scholar
  174. 174.
    Lerich A, Hillmer S, Langhans M, Scheuring D, van Bentum P, Robinson DG (2012) ER import sites and their relationship to ER exit sites: a new model for bidirectional ER-Golgi transport in higher plants. Front Plant Sci 3:143. doi: 10.3389/fpls.2012.00143 PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Pimpl P, Movafeghi A, Coughlan S, Denecke J, Hillmer S, Robinson DG (2000) In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 12:2219–2236. doi:10.1105/tpc.12.11.2219Google Scholar
  176. 176.
    Ritzenthaler C, Nebenführ A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG (2002) Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14:237–261. doi:10.1105/tpc.010237Google Scholar
  177. 177.
    Robinson DG, Herranz MC, Bubeck J, Pepperkok R, Ritzenthaler C (2007) Membrane dynamics in the early secretory pathway. Crit Rev Plant Sci 26:199–225. doi: 10.1080/07352680701495820 CrossRefGoogle Scholar
  178. 178.
    Staehelin LA, Kang BH (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol 147:1454–1468PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Robinson DG, Brandizzi F, Hawes C, Nakano A (2015) Vesicles versus tubes: is endoplasmic reticulum-Golgi transport in plants fundamentally different from other eukaryotes? Plant Physiol 168:393–406. doi: 10.1104/pp.15.00124 PubMedPubMedCentralCrossRefGoogle Scholar
  180. 180.
    Malhotra V, Serafini T, Orci L, Shepherd JC, Rothman JE (1989) Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58:329–336. doi: 10.1016/0092-8674(89)90847-7 PubMedCrossRefGoogle Scholar
  181. 181.
    Serafini T, Stenbeck G, Brecht A, Lottspeich F, Orci L, Rothman JE, Wieland FT (1991) A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature 349:215–220. doi: 10.1038/349215a0 PubMedCrossRefGoogle Scholar
  182. 182.
    Waters MG, Serafini T, Rothman JE (1991) ‘Coatomer’: a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 349:248–251. doi: 10.1038/349248a0 PubMedCrossRefGoogle Scholar
  183. 183.
    Serafini T, Orci L, Amherdt M, Brunner M, Kahn RA, Rothman JE (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. doi: 10.1016/0092-8674(91)90176-Y PubMedCrossRefGoogle Scholar
  184. 184.
    Orci L, Palmer DJ, Ravazzola M, Perrelet A, Amherdt M, Rothman JE (1993) Budding from Golgi membranes requires the coatomer complex of non-clathrin coat proteins. Nature 362:648–652. doi: 10.1038/362648a0 PubMedCrossRefGoogle Scholar
  185. 185.
    Rothman JE, Wieland FT (1996) Protein sorting by transport vesicles. Science 272:227–234. doi: 10.1126/science.272.5259.227 PubMedCrossRefGoogle Scholar
  186. 186.
    Zink S, Wenzel D, Wurm CA, Schmitt HD (2009) A link between ER tethering and COP-I vesicle uncoating. Dev Cell 17:403–416. doi: 10.1016/j.devcel.2009.07.012 PubMedCrossRefGoogle Scholar
  187. 187.
    Hong W (2005) SNAREs and traffic. Biochim Biophys Acta 1744:493–517. doi: 10.1016/j.bbamcr.2005.03.014 PubMedCrossRefGoogle Scholar
  188. 188.
    Klumperman J (2011) Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3:a005181. doi: 10.1101/cshperspect.a005181 PubMedPubMedCentralCrossRefGoogle Scholar
  189. 189.
    Marsh BJ, Volkmann N, McIntosh JR, Howell KE (2004) Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet b cells. Proc Natl Acad Sci 101:5565–5570. doi: 10.1073/pnas.0401242101 PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Trucco A, Polishchuk RS, Martella O, Di Pentima A, Fusella A, Di Giandomenico D, San Pietro E, Beznoussenko GV, Polishchuk EV, Baldassarre M, Buccione R, Geerts WJ, Koster AJ, Burger KN, Mironov AA, Luini A (2004) Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat Cell Biol 6:1071–1081. doi: 10.1038/ncb1180 PubMedCrossRefGoogle Scholar
  191. 191.
    Griffiths G, Pfeiffer S, Simons K, Matlin K (1985) Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J Cell Biol 101:949–964. doi: 10.1083/jcb.101.3.949 PubMedCrossRefGoogle Scholar
  192. 192.
    Griffiths G, Simons K (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234:438–443. doi: 10.1126/science.2945253 PubMedCrossRefGoogle Scholar
  193. 193.
    Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357. doi: 10.1105/tpc.109.072637 PubMedPubMedCentralCrossRefGoogle Scholar
  194. 194.
    Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H + -ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730. doi: 10.1105/tpc.105.037978 PubMedPubMedCentralCrossRefGoogle Scholar
  195. 195.
    Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-Golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319. doi:10.1105/tpc.106.045708Google Scholar
  196. 196.
    Glick BS, Luini A (2011) Models for Golgi traffic: a critical assessment. Cold Spring Harb Perspect Biol 3:a005215. doi: 10.1101/cshperspect.a005215 PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    Rabouille C, Hui N, Hunte F, Kieckbusch R, Berger EG, Warren G, Nilsson T (1995) Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J Cell Sci 108:1617–1627PubMedGoogle Scholar
  198. 198.
    Guo Y, Sirkis DW, Schekman R (2014) Protein sorting at the trans-Golgi network. Annu Rev Cell Dev Biol 30:169–206. doi: 10.1146/annurev-cellbio-100913-013012 PubMedCrossRefGoogle Scholar
  199. 199.
    Simmen T, Honing S, Icking A, Tikkanen R, Hunziker W (2002) AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat Cell Biol 4:154–159. doi:doi: 10.1038/ncb745
  200. 200.
    Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, Rodriguez-Boulan E (2012) The clathrin adaptor AP-1A mediates basolateral polarity. Dev Cell 22:811–823. doi: 10.1016/j.devcel.2012.02.004 PubMedPubMedCentralCrossRefGoogle Scholar
  201. 201.
    Bonifacino JS (2014) Adaptor proteins involved in polarized sorting. J Cell Biol 204:7–17. doi: 10.1083/jcb.201310021 PubMedPubMedCentralCrossRefGoogle Scholar
  202. 202.
    Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572. doi: 10.1038/42408 PubMedCrossRefGoogle Scholar
  203. 203.
    Bard F, Malhotra V (2006) The formation of TGN-to-plasma-membrane transport carriers. Annu Rev Cell Dev Biol 22:439–455. doi: 10.1146/annurev.cellbio.21.012704.133126 PubMedCrossRefGoogle Scholar
  204. 204.
    Wang CW, Hamamoto S, Orci L, Schekman R (2006) Exomer: a coat complex for transport of select membrane proteins from the trans-Golgi network to the plasma membrane in yeast. J Cell Biol 174:973–983. doi: 10.1083/jcb.200605106 PubMedPubMedCentralCrossRefGoogle Scholar
  205. 205.
    Sanchatjate S, Schekman R (2006) Chs5/6 complex: a multiprotein complex that interacts with and conveys chitin synthase III from the trans-Golgi network to the cell surface. Mol Biol Cell 17:4157–4166. doi: 10.1091/mbc.E06-03-0210 PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    Barfield RM, Fromme JC, Schekman R (2009) The exomer coat complex transports Fus1p to the plasma membrane via a novel plasma membrane sorting signal in yeast. Mol Biol Cell 20:4985–4996. doi: 10.1091/mbc.E09-04-0324 PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Paczkowski JE, Richardson BC, Strassner AM, Fromme JC (2012) The exomer cargo adaptor structure reveals a novel GTPase-binding domain. EMBO J 31:4191–4203. doi: 10.1038/emboj.2012.268 PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    Starr TL, Pagant S, Wang CW, Schekman R (2012) Sorting signals that mediate traffic of chitin synthase III between the TGN/endosomes and to the plasma membrane in yeast. PLoS One 7, e46386. doi: 10.1371/journal.pone.0046386 PubMedPubMedCentralCrossRefGoogle Scholar
  209. 209.
    Santos B, Snyder M (2003) Specific protein targeting during cell differentiation: polarized localization of Fus1p during mating depends on Chs5p in Saccharomyces cerevisiae. Eukaryot Cell 2:821–825. doi: 10.1128/EC.2.4.821-825.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    Trautwein M, Schindler C, Gauss R, Dengjel J, Hartmann E, Spang A (2006) Arf1p, Chs5p and the ChAPs are required for export of specialized cargo from the Golgi. EMBO J 25:943–954. doi: 10.1038/sj.emboj.7601007 PubMedPubMedCentralCrossRefGoogle Scholar
  211. 211.
    Goud B, Salminen A, Walworth NC, Novick PJ (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53:753–768. doi: 10.1016/0092-8674(88)90093-1 PubMedCrossRefGoogle Scholar
  212. 212.
    Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5:518–528. doi: 10.1016/S1369-5266(02)00307-2 PubMedCrossRefGoogle Scholar
  213. 213.
    Gendre D, Oh J, Boutté Y, Best JG, Samuels L, Nilsson R, Uemura T, Marchant A, Bennett MJ, Grebe M, Bhalerao RP (2011) Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation. Proc Natl Acad Sci U S A 108:8048–8053. doi: 10.1073/pnas.1018371108 PubMedPubMedCentralCrossRefGoogle Scholar
  214. 214.
    Gendre D, McFarlane HE, Johnson E, Mouille G, Sjödin A, Oh J, Levesque-Tremblay G, Watanabe Y, Samuels L, Bhalerao RP (2013) Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis. Plant Cell 25:2633–2646. doi: 10.1105/tpc.113.112482 PubMedPubMedCentralCrossRefGoogle Scholar
  215. 215.
    McFarlane HE, Döring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94. doi: 10.1146/annurev-arplant-050213-040240 PubMedCrossRefGoogle Scholar
  216. 216.
    Boutté Y, Jonsson K, McFarlane HE, Johnson E, Gendre D, Swarup R, Friml J, Samuels L, Robert S, Bhalerao RP (2014) ECHIDNA-mediated post-Golgi trafficking of auxin carriers for differential cell elongation. Proc Natl Acad Sci U S A 110:16259–16264. doi: 10.1073/pnas.1309057110 CrossRefGoogle Scholar
  217. 217.
    Jürgens G (2005) Plant cytokinesis: Fission by fusion. Trends Cell Biol 15:277–283. doi: 10.1016/j.tcb.2005.03.005 PubMedCrossRefGoogle Scholar
  218. 218.
    Müller S, Jürgens G (2015) Plant cytokinesis-No ring, no constriction but centrifugal construction of the partitioning membrane. Semin Cell Dev Biol. doi: 10.1016/j.semcdb.2015.10.037 PubMedGoogle Scholar
  219. 219.
    Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71. doi: 10.1016/S0092-8674(00)80993-9 PubMedCrossRefGoogle Scholar
  220. 220.
    Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 139:1485–1493. doi: 10.1083/jcb.139.6.1485 PubMedPubMedCentralCrossRefGoogle Scholar
  221. 221.
    Assaad FF, Huet Y, Mayer U, Jürgens G (2001) The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE. J Cell Biol 152:531–543. doi: 10.1083/jcb.152.3.531 PubMedPubMedCentralCrossRefGoogle Scholar
  222. 222.
    Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155:239–249. doi: 10.1083/jcb.200107126 PubMedPubMedCentralCrossRefGoogle Scholar
  223. 223.
    Hammer JA 3rd, Wu XS (2002) Rabs grab motors: defining the connections between Rab GTPases and motor proteins. Curr Opin Cell Biol 14:69–75. doi: 10.1016/S0955-0674(01)00296-4 PubMedCrossRefGoogle Scholar
  224. 224.
    TerBush DR, Maurice T, Roth D, Novick P (1996) The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15:6483–6494PubMedPubMedCentralGoogle Scholar
  225. 225.
    Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12:671–682. doi: 10.1016/j.devcel.2007.04.005 PubMedCrossRefGoogle Scholar
  226. 226.
    Zárský V, Kulich I, Fendrych M, Pečenková T (2013) Exocyst complexes multiple functions in plant cells secretory pathways. Curr Opin Plant Biol 16:726–733. doi: 10.1016/j.pbi.2013.10.013 PubMedCrossRefGoogle Scholar
  227. 227.
    Borgonovo B, Ouwendijk J, Solimena M (2006) Biogenesis of secretory granules. Curr Opin Cell Biol 18:365–370. doi: 10.1016/j.ceb.2006.06.010 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Institute of Biochemistry and Biology, Plant PhysiologyUniversity of PotsdamPotsdamGermany

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