Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae

Journal of Cell Biology

Volumn 145, Issue 1, 1999, Pages 69-81

  Rossanese, Olivia W ^a   Soderholm, Jon ^a   Bevis, Brooke J ^a   Sears, Irina B ^a   O'Connor, James ^a   Williamson, Edward K ^a   Glick, Benjamin S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Apparatus, Golgi; Endoplasmic reticulum Pichia; Microtubules; Saccharomyces

Indexed keywords

MEMBRANE PROTEIN; NOCODAZOLE; PROTEIN SEC12P; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; MEMBRANE VESICLE; MICROTUBULE; NONHUMAN; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; SPECIES DIFFERENCE;

CARRIER PROTEINS; CELL CYCLE; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GENES, REPORTER; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; LUMINESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; NOCODAZOLE; PHOSPHOPROTEINS; PICHIA; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECIES SPECIFICITY; VESICULAR TRANSPORT PROTEINS;

PICHIA; PICHIA PASTORIS; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0033526048     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.1.69     Document Type: Article

References (96)

1. Acharya, U., A. Mallabiabarrena, J.K. Acharya, and V. Malhotra. 1998. Signaling via mitogen-activated protein kinase (MEK1) is required for Golgi fragmentation during mitosis. Cell. 92:183-192.
2. 2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell. 3:633-654.
3. Ayscough, K., N.M.A. Hajibagheri, R. Watson, and G. Warren. 1993. Stacking of Golgi cisternae in Schizosaccharomyces pombe requires intact microtubules. J. Cell Sci. 106:1227-1237.
4. Bannykh, S.I., and W.E. Balch. 1997. Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138:1-4.
5. Barlowe, C., and R. Schekman. 1993. SEC12 encodes a guanine-nucleotide-exchange factor essential for transport vesicle budding from the ER. Nature. 365:347-349.
6. Barr, F.A., M. Puype, J. Vandekerckhove, and G. Warren. 1997. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell. 91:253-262.
7. Beams, H.W., and R.G. Kessel. 1968. The Golgi apparatus: structure and function. Int. Rev. Cytol. 23:209-276.
8. Bénédetti, H., S. Raths, F. Crusaz, and H. Riezman. 1994. The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell. 5:1023-1037.
9. Boevink, P., K. Oparka, S. Santa Cruz, B. Martin, A. Betteridge, and C. Hawes. 1998. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15:441-447.
10. Bonfanti, L., A.A. Mironov, Jr., J. Martínez-Menárguez, O. Martella, A. Fusella, M. Baldassarre, R. Buccione, H.J. Geuze, A.A. Mironov, and A. Luini. 1998. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell. 95:993-1003.
11. Bracker, C.E., D.J. Morré, and S.N. Grove. 1996. Structure, differentiation and multiplication of Golgi apparatus in fungal hyphae. Protoplasma. 194:250-274.
12. Burkhardt, J.K. 1998. The role of microtubule-based motor proteins in maintaining the structure and function of the Golgi complex. Biochim. Biophys. Acta. 1404:113-126.
13. Chapman, R.E., and S. Munro. 1994. The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANPI, a member of a new family of genes affecting the secretory pathway. EMBO (Eur. Mol. Biol. Organ.) J. 13: 4896-4907.
14. Chappell, T.G., and G. Warren. 1989. A galactosyltransferase from the fission yeast Schizosaccharomyces pombe. J. Cell Biol. 109:2693-2702.
15. Clamp, J.R., and L. Hough. 1965. The periodate oxidation of amino acids with reference to studies of glycoproteins. Biochem. J. 94:17-24.
16. Cluett, E.B., and W.J. Brown. 1992. Adhesion of Golgi cisternae by proteinaceous interactions: intercisternal bridges as putative adhesive structures. J. Cell Sci. 103:773-784.
17. Cole, N.B., N. Sciaky, A. Marotta, J. Song, and J. Lippincott-Schwartz. 1996. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell. 7:631-650.
18. Driouich, A., and L.A. Staehelin. 1997. The plant Golgi apparatus: structural organization and functional properties. In The Golgi Apparatus. E.G. Berger and J. Roth, editors. Birkhäuser, Basel, Switzerland, 275-301.
19. Dunphy, W.G., and J.E. Rothman. 1985. Compartmental organization of the Golgi stack. Cell. 42:13-21.
20. Farquhar, M.G. 1985. Progress in unraveling pathways of Golgi traffic. Annu. Rev. Cell Biol. 1:447-488.
21. Farquhar, M.G., and G.E. Palade. 1981. The Golgi apparatus (complex) -(1954-1981) - from artifact to center stage. J. Cell Biol. 91:77s-103s.
22. Franzusoff, A., K. Redding, J. Crosby, R.S. Fuller, and R. Schekman. 1991. Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112:27-37.
23. Gaynor, E.C., and S.D. Emr. 1997. COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136:789-802.
24. Gaynor, E.C., S. te Heesen, T.R. Graham, M. Aebi, and S.D. Emr. 1994. Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast. J. Cell Biol. 127:653-665.
25. Glick, B.S. 1996. Cell biology: alternatives to baker's yeast. Curr. Biol. 6:1570-1572.
26. Glick, B.S., and V. Malhotra. 1998. The curious status of the Golgi apparatus. Cell. 95:883-889.
27. Gould, S.J., D. McCollum, A.P. Spong, J.A. Heyman, and S. Subramani. 1992. Development of the yeast Pichia pastoris as a model organism for a genetic and molecular analysis of peroxisome assembly. Yeast. 8:613-628.
28. Griffiths, G. 1993. Fine Structure Immunocytochemistry. Springer-Verlag, Berlin. 459 pp.
29. Harris, S.L., and M.G. Waters. 1996. Localization of a yeast early Golgi mannosyltransferase, Och1p, involves retrograde transport. J. Cell Biol. 132:985-998.
30. Hell, S.W., and E.H.K. Stelzer. 1995. Lens aberrations in confocal fluorescence microscopy. In Handbook of Biological Confocal Microscopy. J.B. Pawley, editor. Plenum Publishing Corp., New York. 347-354.
31. Higgins, D.R., and J.M. Cregg. 1998. Pichia Protocols. Methods in Molecular Biology. Vol. 103. J.M. Walker, editor. Humana Press, Totowa, NJ. 270 pp.
32. Jacobs, C.W., A.E.M. Adams, P.J. Szaniszlo, and J.R. Pringle. 1988. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 107: 1409-1426.
33. Kaiser, C.A., and R. Schekman. 1990. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell. 61: 723-733.
34. Kärgel, E., R. Menzel, H. Honeck, F. Vogel, A. Böhmer, and W.-H. Schunck. 1996. Candida maltosa NADPH-cytochrome P450 reductase: cloning of a full-length cDNA, heterologous expression in Saccharomyces cerevisiae and function of the N-terminal region for membrane anchoring and proliferation of the endoplasmic reticulum. Yeast. 12:333-348.
35. Kreis, T.E. 1990. Role of microtubules in the organisation of the Golgi apparatus. Cell Motil. Cytoskelet. 15:67-70.
36. Kuehn, M.J., and R. Schekman. 1997. COPII and secretory cargo capture into transport vesicles. Curr. Opin. Cell Biol. 9:477-483.
37. Kuge, O., C. Dascher, L. Orci, T. Rowe, M. Amherdt, H. Plutner, M. Ravazzola, G. Tanigawa, J.E. Rothman, and W.E. Balch. 1994. Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125:51-65.
38. Lacey, A.J. 1989. Light Microscopy in Biology. A Practical Approach. IRL Press, Oxford, UK. 329 pp.
39. Lew, D.J., T. Weinert, and J.R. Pringle. 1997. Cell cycle control in Saccharomyces cerevisiae. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Vol. 3. J.R. Pringle, J.R. Broach, and E.W. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 607-695.
40. Lippincott-Schwartz, J. 1998. Cytoskeletal proteins and Golgi dynamics. Curr. Opin. Cell Biol. 10:52-59.
41. Love, H.D., C.-C. Lin, C.S. Short, and J. Ostermann. 1998. Isolation of functional Golgi-derived vesicles with a possible role in retrograde transport. J. Cell Biol. 140:541-551.
42. Lupashin, V.V., S. Hamamoto, and R.W. Schekman. 1996. Biochemical requirements for the targeting and fusion of ER-derived transport vesicles with purified yeast Golgi membranes. J. Cell Biol. 132:277-289.
43. Lussier, M., A.M. Sdicu, T. Ketela, and H. Bussey. 1995. Localization and targeting of the Saccharomyces cerevisiae Kre2p/Mnt1p α1,2-mannosyltransferase to a medial-Golgi compartment. J. Cell Biol. 131:913-927.
44. Makarow, M. 1988. Secretion of invertase in mitotic yeast cells. EMBO (Eur. Mol. Biol. Organ.) J. 7:1475-1482.
45. Mironov, A.A., P. Weidman, and A. Luini. 1997. Variations on the intracellular transport theme: maturing cisternae and trafficking tubules. J. Cell Biol. 138: 481-484.
46. Mollenhauer, H.H., and D.J. Morré. 1978. Structural compartmentation of the cytosol: zones of exclusion, zones of adhesion, cytoskeletal and intercisternal elements. Subcell. Biochem. 5:327-359.
47. Mollenhauer, H.H., and D.J. Morré. 1991. Perspectives on Golgi apparatus form and function. J. Electron Microsc. Tech. 17:2-14.
48. Morré, D.J. 1987. The Golgi apparatus. Int. Rev. Cytol. 17:211-253.
49. Nakanishi-Shindo, Y., K. Nakayama, A. Tanaka, Y. Toda, and Y. Jigami. 1993. Structure of the N-linked oligosaccharides that show the complete loss of α-1,6-polymannose outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 268:26338-26345.
50. Nakano, A., D. Brada, and R. Schekman. 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.
51. Nakano, A., and M. Muramatsu. 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.
52. Nakayama, K., T. Nagasu, Y. Shimma, J. Kuromitsu, and Y. Jigami. 1992. OCHI encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagine-linked oligosaccharides. EMBO (Eur. Mol. Biol. Organ.) J. 11:2511-2519.
53. Nishikawa, S., and A. Nakano. 1991. The GTP-binding Sar1 protein is localized to the early compartment of the yeast secretory pathway. Biochem. Biophys. Acta. 1093:135-143.
54. Nishikawa, S., and A. Nakano. 1993. Identification of a gene required for membrane protein retention in !he early secretory pathway. Proc. Natl. Acad. Sci. USA. 90:8179-8183.
55. Nishikawa, S.-I., A. Hirata, and A. Nakano. 1994. Inhibition of endoplasmic reticulum (ER)-to-Golgi transport induces relocalizalion of binding protein (BiP) within the ER to form the BiP bodies. Mol. Biol. Cell. 5:1129-1143.
56. Novick, P., C. Field, and R. Schekman. 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell. 21:205-215.
57. Orci, L., M. Ravazzola, P. Meda, C. Holcomb, H.-P. Moore, L. Hicke, and R. Schekman. 1991. Mammalian Sec23p homologue is restricted to the endoplasmic reticulum transitional cytoplasm. Proc. Natl. Acad. Sci. USA. 88: 8611-8615.
58. Orlean, P. 1997. Biogenesis of yeast wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Vol. 3. J.R. Pringle, J.R. Broach, and E.W. Jones, editors, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 229-362.
59. Paccaud, J.-P., W. Reith, J.-L. Carpentier, M. Ravazzola, M. Amherdt, R. Schekman, and L. Orci. 1996. Cloning and functional characterization of mammalian homologues of the COPII component Sec23. Mol. Biol. Cell. 7:1535-1546.
60. Palade, G. 1975. Intracellular aspects of the process of protein synthesis. Science. 189:347-358.
61. Pelham, H.R.B. 1998. Getting through the Golgi complex. Trends Cell Biol. 8:45-49.
62. Presley, J.F., N.B. Cole, T.A. Schroer, K. Hirschherg, K.J.M. Zaal, and J. Lippincott-Schwartz. 1997. ER-to-Golgi transport visualized in living cells. Nature. 389:81-85.
63. Preuss, D., J. Mulholland, A. Franzusoff, N. Segev, and D. Botstein. 1992. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoeleclron microscopy. Mol. Biol. Cell. 3:789-803.
64. Preuss, D., J. Mulholland, C.A. Kaiser, P. Orlean, C. Albright, M.D. Rose, P.W. Robbins, and D. Botstein. 1991. Structure of the yeast endoplasmic reticulum: localization of ER proteins using immunofluorescence and immunoelectron microscopy. Yeast. 7:891-911.
65. Pringle, J.R., A.E.M. Adams, D.G. Drubin, and B.K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565-602.
66. Pryer, N.K., N.R. Salama, R. Schekman, and C.A. Kaiser. 1993. Cytosolic Sec13p complex is required for vesicle formation from the endoplasmic reticulum in vitro. J. Cell Biol. 120:865-875.
67. Rabouille, C., and G. Warren. 1997. Changes in the architecture of the Golgi apparatus during mitosis. In The Golgi Apparatus. E.G. Berger and J. Roth, editors. Birkhäuser, Basel, Switzerland, 195-217.
68. Ramhourg, A., Y. Clermont, and F. Képès. 1993. Modulation of the Golgi apparatus in Saccharomyces cerevisiae sec7 mutants as seen by three-dimensional electron microscopy. Anat. Rec. 237:441-452.
69. Rambourg, A., Y. Clermont, J.M. Nicaud, C. Gaillardin, and F. Kepes. 1996. Transformations of membrane-bound organelles in sec14 mutants of the yeasts Sacchammvces cerevisiae and Yarrowia lipolytica. Anat. Rec. 245: 447-458.
70. Rambourg, A., Y. Clermont, L. Ovtracht, and F. Képès. 1995. Three-dimensional structure of tubular networks, presumably Golgi in nature, in various yeast strains: a comparative study. Anat. Rec. 243:283-293.
71. Redding, K., C. Holcomb, and R.S. Fuller. 1991. Immunolocalization of Kex2 protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. J. Cell Biol. 113:527-538.
72. Rieder, S.E., L.M. Banta, K. Köhrer, J.M. McCaffery, and S.D. Emr. 1996. Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell. 7:985-999.
73. Rose, M.D., L.M. Misra, and J.P. Vogel. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell. 57:1211-1221.
74. Rothman, J.E., and F.T. Wieland. 1996. Protein sorting by transport vesicles. Science. 272:227-234.
75. Rothstein, R. 1991. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194:281-301.
76. Rowe, T., C. Dascher, S. Bannykh, H. Plutner, and W.E. Balch. 1998. Role of vesicle-associated syntaxin 5 in the assembly of pre-Golgi intermediates. Science. 279:696-700.
77. Scales, S.J., R. Pepperkok, and T.E. Kreis. 1997. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPH and COPI. Cell. 90:1137-1148.
78. Schnepf, E. 1993. Golgi apparatus and slime secretion in plants: the early implications and recent models of membrane traffic. Protoplasma. 172:3-11.
79. Sears, I.B., J. O'Connor, O.W. Rossanese, and B.S. Glick. 1998. A versatile set of vectors for constitutive and regulated gene expression in Pichia pastoris. Yeast. 14:783-790.
80. Segev, N., and D. Botstein. 1987. The ras-like yeast YPT1 gene is itself essential for growth, sporulation, and starvation response. Mol. Cell. Biol. 7:2367-2377.
81. Segev, N., J. Mulholland, and D. Botstein. 1988. The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell. 52:915-924.
82. Shaywitz, D.A., L. Orci, M. Ravazzola, A. Swaroop, and C.A. Kaiser. 1995. Human SEC13Rp functions in yeast and is located on transport vesicles budding from the endoplasmic reticulum. J. Cell Biol. 128:769-777.
83. Sitia, R., and J. Meldolesi. 1992. Endoplasmic reticulum: a dynamic patchwork of specialized subregions. Mol. Biol. Cell. 3:1067-1072.
84. Staehelin, L.A., and I. Moore. 1995. The plant Golgi apparatus: structure, functional organization and trafficking mechanisms. Annu. Rev. Plain Physiol. Plant Mol. Biol. 46:261-288.
85. Stanley, H., J. Botas, and V. Malhotra. 1997. The mechanism of Golgi segregation during mitosis is cell type-specific. Proc. Natl. Acad. Sci. USA. 94: 14467-14470.
86. Storrie, B., J. White, S. Röttger, E.H.K. Stelzer, T. Suganuma, and T. Nilsson. 1998. Recycling of Golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. J. Cell Biol. 143:1505-1521.
87. Svodoba, A., and O. Necas. 1987. Ultrastructure of Saccharomyces cerevisiae cells accumulating Golgi organelles. J. Basic Microbiol. 27:603-612.
88. Tang, B.L., F. Peter, J. Krijnse-Locker, S. Low, G. Griffiths, and W. Hong. 1997. The mammalian homolog of yeast Sec13p is enriched in the intermediate compartment and is essential for protein transport from the endoplasmic reliculum to the Golgi apparatus. Mol. Cell. Biol. 17:256-266.
89. Thyberg, J., and S. Moskalewski. 1985. Microtubules and the organization of the Golgi complex. Exp. Cell Res. 159:1-16.
90. Tokuyasu, K.T. 1989. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy. Histochem. J. 21:163-171.
91. Trimble, R.B., P.H. Atkinson, J.F. Tschopp, R.R. Townsend, and F. Maley. 1991. Structure of oligosaccharides on Saccharomyces SUC2 invertase secreted by the methylotrophic yeast Pichia pastoris. J. Biol. Chem. 266:22807-22817.
92. Waterham, H.R., M.E. Digan, P.J. Koutz, S.V. Lair, and J.M. Cregg. 1997. Isolation of the Pichia pastoris glyceraldehyde-3-phosphate dehydrogenase gene and characterization of its promoter. Gene. 186:37-44.
93. Weiss, D.G., W. Maile, and R.A. Wick. 1989. Video microscopy. In Light Microscopy in Biology. A Practical Approach, A.J. Lacey, editor. IRL Press, Oxford, UK. 221-278.
94. Whaley, W.G. 1975. The Golgi Apparatus. Springer-Verlag, Vienna, 190 pp.
95. Wolf, J., M. Nicks, S. Deitz, E. van Tuinen, and A. Franzusoff. 1998. An N-end rule destabilization mutant reveals pre-Golgi requirements for Sec7p in yeast membrane traffic. Biochem. Biophys. Res. Commun. 243:191-198.
96. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 33:103-119.