Deficiencies in the endoplasmic reticulum (ER)-membrane protein Gab1p perturb transfer of glycosylphosphatidylinositol to proteins and cause perinuclear ER-associated actin bar formation

Molecular Biology of the Cell

Volumn 15, Issue 6, 2004, Pages 2758-2770

  Grimme, Stephen J ^a   Gao, Xiang Dong ^b   Martin, Paul S ^b   Tu, Kim ^b   Tcheperegine, Serguei E ^b   Corrado, Kathleen ^c,d   Farewell, Anne E ^c,e   Orlean, Peter ^a   Bi, Erfei ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Center for Forensic Sciences   (United States)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMIDINOTRANSFERASE; GAB1P PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN LOCALIZATION; TEMPERATURE; TEMPERATURE SENSITIVITY;

ACTINS; ACYLTRANSFERASES; ALLELES; AMINO ACID SEQUENCE; CELL MEMBRANE; CELL POLARITY; CLONING, MOLECULAR; CONSERVED SEQUENCE; ENDOPLASMIC RETICULUM; GENE DELETION; GENES, ESSENTIAL; GLYCOSYLPHOSPHATIDYLINOSITOLS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 2542460173     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-01-0035     Document Type: Article

References (73)

1. Adams, A.E.M., and Pringle, J.R. (1984). Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J. Cell Biol. 98, 934-945.
2. Ashworth, S.L., Southgate, E.L., Sandoval, R.M., Meberg, P.J., Bamburg, J.R., and Molitoris, B.A. (2003). ADF/cofilin mediates actin cytoskeletal alterations in LLC-PK cells during ATP depletion. Am. J. Physiol. 284, F852-F862.
3. Bamburg, J.R., McGough, A., and Ono, S. (1999). Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol. 9, 364-370.
4. Baumann, O. (1998). Association of spectrin with a subcompartment of the endoplasmic reticulum in Honeybee photoreceptor cells. Cell Motil. Cytoskeleton 41, 74-86.
5. Benachour, A., Sipos, G., Flury, I., Reggiori, F., Canivenc-Gansel, E., Vionnet, C., Conzelmann, A., and Benghezal, M. (1999). Deletion of GPI7, a yeast gene required for addition of a side chain to the glycosylphosphatidylinositol (GPI) core structure, affects GPI protein transport, remodeling, and cell wall integrity. J. Biol. Chem. 274, 15251-15261.
6. Benghezal, M., Benachour, A., Rusconi, S., Aebi, M., and Conzelmann, A. (1996). Yeast Gpi8p is essential for GPI anchor attachment onto proteins. EMBO J. 15, 6575-6583.
7. Bi, E., and Pringle, J.R. (1996). ZDS1 and ZDS2, genes whose products may regulate Cdc42p in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5264-5275.
8. Boldogh, I.R., Yang, H.C., and Pon, L.A. (2001). Mitochondrial inheritance in budding yeast. Traffic 2, 368-374.
9. Cadwell, R.C., and Joyce, G.F. (1992). Randomization of genes by PCR mutagenesis. PCR Methods Appl. 2, 28-33.
10. Carlson, M., and Botstein, D. (1982). Two differentially regulated mRNAs with different 5′ ends encode secreted and intracellular forms of yeast invertase. Cell 28, 145-154.
11. Caro, L.H., Tettelin, H., Vossen, J.H., Ram, A.F., van den Ende, H., and Klis, F.M. (1997). In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13, 1477-1489.
12. Catlett, N.L., Duex, J.E., Tang, F., and Weisman, L.S. (2000). Two distinct regions in a yeast myosin-V tail domain are required for the movement of different cargoes. J. Cell Biol. 150, 513-526.
13. Caviston, J.P., Tcheperegine, S.E., and Bi, E. (2002). Singularity in budding: a role for the evolutionarily conserved small GTPase Cdc42p. Proc. Natl. Acad. Sci. USA 99, 12185-12190.
14. Drubin, D.G., Miller, K.G., and Botstein, D. (1988). Yeast actin-binding proteins: evidence for a role in morphogenesis. J. Cell Biol. 107, 2551-2561.
15. Eisenhaber, B., Bork, P., and Eisenhaber, F. (2001). Post-translational GPI lipid anchor modification of proteins in kingdoms of life: analysis of protein sequence data from complete genomes. Protein Eng. 14, 17-25.
16. Eisenhaber, B., Maurer-Stroh, S., Novatchkova, M., Schneider, G., and Eisenhaber, F. (2003). Enzymes and auxiliary factors for GPI lipid anchor biosynthesis and post-translational transfer to proteins. Bioessays 25, 367-385.
17. Estrada, P., Kim, J., Coleman, J., Walker, L., Dunn, B., Takizawa, P., Novick, P., and Ferro-Novick, S. (2003). Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163, 1255-1266.
18. Fehrenbacher, K.L., Davis, D., Wu, M., Boldogh, I., and Pon, L.A. (2002). Endoplasmic reticulum dynamics, inheritance, and cytoskeletal interactions in budding yeast. Mol. Biol. Cell 13, 854-865.
19. Finger, F.P., Hughes, T.E., and Novick, P. (1998). Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92, 559-71.
20. Fraering, P., Imhof, I., Meyer, U., Strub, J.M., van Dorsselaer, A., Vionnet, C., and Conzelmann, A. (2001). The GPI transamidase complex of Saccharomyces cerevisiae contains Gaa1p, Gpi8p, and Gpi16p. Mol. Biol. Cell 12, 3295-3306.
21. Gaynor, E.C., Mondesert, G., Grimme, S.J., Reed, S.I., Orlean, P., and Emr, S.D. (1999). MCD4 encodes a conserved endoplasmic reticulum membrane protein essential for glycosylphosphatidylinositol anchor synthesis in yeast. Mol. Biol. Cell 10, 627-648.
22. Gietz, R.D., and Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
23. Grimme, S.J., Westfall, B.A., Wiedman, J.M., Taron, C.H., and Orlean, P. (2001). The essential Smp3 protein is required for addition of the side-branching fourth mannose during assembly of yeast glycosylphosphatidylinositols. J. Biol. Chem. 276, 27731-27739.
24. Haarer, B.K., Lillie, S.H., Adams, A.E., Magdolen, V., Bandlow, W., and Brown, S.S. (1990). Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110, 105-114.
25. Haarer, B.K., Petzold, A.S., and Brown, S.S. (1993). Mutational analysis of yeast profilin. Mol. Cell. Biol. 13, 7864-7873.
26. Hamada, K., Terashima, H., Arisawa, M., Yabuki, N., and Kitada, K. (1999). Amino acid residues in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J. Bacteriol. 181, 3886-3889.
27. Hamburger, D., Egerton, M., and Riezman, H. (1995). Yeast Gaa1p is required for attachment of a completed GPI anchor onto proteins. J. Cell Biol. 129, 629-639.
28. Hill, J.E., Myers, A.M., Koerner, T.J., and Tzagoloff, A. (1986). Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2, 163-167.
29. Hong, Y., Ohishi, K., Kang, J.Y., Tanaka, S., Inoue, N., Nishimura, J., Maeda, Y., and Kinoshita, T. (2003). Human PIG-U and yeast Cdc91p are the fifth subunit of GPI transamidase that attaches GPI-anchors to proteins. Mol. Biol. Cell 14, 1780-1789.
30. Huffaker, T.C., and Robbins, P.W. (1983). Yeast mutants deficient in protein glycosylation. Proc. Natl. Acad. Sci. USA 80, 7466-7470.
31. 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.
32. Karpova, T.S., Lepetit, M.M., and Cooper, J.A. (1993). Mutations that enhance the cap2 null mutant phenotype in Saccharomyces cerevisiae affect the actin cytoskeleton, morphogenesis and pattern of growth. Genetics 135, 693-709.
33. Kinoshita, T., Inoue, N., and Takeda, J. (1995). Defective glycosylphosphatidylinositol anchor synthesis and paroxysmal nocturnal hemoglobinuria. Adv. Immunol. 60, 57-103.
34. Kruse, C., Jaedicke, A., Beaudouin, J., Bohl, F., Ferring, D., Guttler, T., Ellenberg, J., and Jansen, R.P. (2002). Ribonucleoprotein-dependent localization of the yeast class V myosin Myo4p. J. Cell Biol. 159, 971-982.
35. Leidich, S.D., Kostova, Z., Latek, R.R., Costello, L.C., Drapp, D.A., Gray, W., Fassler, J.S., and Orlean, P. (1995). Temperature-sensitive yeast GPI anchoring mutants gpi2 and gpi3 are defective in the synthesis of N-acetylglucosaminyl phosphatidylinositol. Cloning of the GPI2 gene. J. Biol. Chem. 270, 13029-13035.
36. Leidich, S.D., and Orlean, P. (1996). Gpi1, a Saccharomyces cerevisiae protein that participates in the first step in glycosylphosphatidylinositol anchor synthesis. J. Biol. Chem. 271, 27829-27837.
37. Lillie, S.H., and Pringle, J.R. (1980). Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J. Bacteriol. 143, 1384-1394.
38. Lipke, P.N., and Ovalle, R. (1998). Cell wall architecture in yeast: new structure and new challenges. J. Bacteriol. 180, 3735-3740.
39. Lipke, P.N., Wojciechowicz, D., and Kurjan, J. (1989). AG alpha 1 is the structural gene for the Saccharomyces cerevisiae alpha-agglutinin, a cell surface glycoprotein involved in cell-cell interactions during mating. Mol. Cell. Biol. 9, 3155-3165.
40. Liu, H., Krizek, J., and Bretscher, A. (1992). Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics 132, 665-673.
41. Liu, H.P., and Bretscher, A. (1989). Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57, 233-242.
42. Longtine, M.S., McKenzie, A., III, DeMarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J.R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
43. McConville, M.J., and Ferguson, M.A. (1993). The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem. J. 294, 305-324.
44. McGough, A., Pope, B., Chiu, W., and Weeds, A. (1997). Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138, 771-781.
45. Meyer, U., Benghezal, M., Imhof, I., and Conzelmann, A. (2000). Active site determination of Gpi8p, a caspase-related enzyme required for glycosylphosphatidylinositol anchor addition to proteins. Biochemistry 39, 3461-3471.
46. Minamide, L.S., Striegl, A.M., Boyle, J.A., Meberg, P.J., and Bamburg, J.R. (2000). Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol. 2, 628-636.
47. Mitchell, D.A., Marshall, T.K., and Deschenes, R.J. (1993). Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast 9, 715-723.
48. Moon, A.L., Janmey, P.A., Louie, K.A., and Drubin, D.G. (1993). Cofilin is an essential component of the yeast cortical cytoskeleton. J. Cell Biol. 120, 421-435.
49. Nagamune, K., Ohishi, K., Ashida, H., Hong, Y., Hino, J., Kangawa, K., Inoue, N., Maeda, Y., and Kinoshita, T. (2003). GPI transamidase of Trypanosoma brucei has two previously uncharacterized (trypanosomatid transamidase 1 and 2) and three common subunits. Proc. Natl. Acad. Sci. USA 100, 10682-10687.
50. Nosjean, O., Briolay, A., and Roux, B. (1997). Mammalian GPI proteins: sorting, membrane residence and functions. Biochim. Biophys. Acta 1331, 153-186.
51. Novick, P., and Botstein, D. (1985). Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 40, 405-416.
52. Ohishi, K., Inoue, N., and Kinoshita, T. (2001). PIG-S and PIG-T, essential for GPI anchor attachment to proteins, form a complex with GAA1 and GPI8. EMBO J. 20, 4088-4098.
53. Ohishi, K., Nagamune, K., Maeda, Y., and Kinoshita, T. (2003). Two subunits of glycosylphosphatidylinositol transamidase, GPI8 and PIG-T, form a functionally important intermolecular disulfide bridge. J. Biol. Chem. 278, 13959-13967.
54. Orlean, P. (1997). Biogenesis of yeast wall and surface components. In: The Molecular and Cellular Biology of the Yeast Saccharomyces. Cell Cycle and Cell Biology, vol. 3, ed. J.R. Pringle, J.R. Broach, and E.W. Jones, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 229-362.
55. Popolo, L., and Vai, M. (1999). The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim. Biophys. Acta 1426, 385-400.
56. Preuss, D., Mulholland, J., Kaiser, C.A., Orlean, P., Albright, C., Rose, M.D., Robbins, P.W., and Botstein, D. (1991). Structure of the yeast endoplasmic reticulum: localization of ER proteins using immunofluorescence and immunoelectron microscopy. Yeast 7, 891-911.
57. Pringle, J.R., Adams, A.E.M., Drubin, D.G., and Haarer, B.K. (1991). Immunofluorescence methods for yeast. Methods Enzymol. 194, 565-602.
58. Prinz, W.A., Grzyb, L., Veenhuis, M., Kahana, J.A., Silver, P.A., and Rapoport, T.A. (2000). Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 150, 461-474.
59. Pruyne, D., and Bretscher, A. (2000). Polarization of cell growth in yeast. J. Cell Sci. 113, 571-585.
60. Pruyne, D.W., Schott, D.H., and Bretscher, A. (1998). Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143, 1931-1945.
61. Riles, L., and Olson, M.V. (1988). Nonsense mutations in essential genes of Saccharomyces cerevisiae. Genetics 118, 601-607.
62. Rivero, F., Kuspa, A., Brokamp, R., Matzner, M., and Noegel, A.A. (1998). Interaptin, an actin-binding protein of the alpha-actinin superfamily in Dictyostelium discoideum, is developmentally and cAMP-regulated and associates with intracellular membrane compartments. J. Cell Biol. 142, 735-750.
63. Rodriguez-Pena, J.M., Cid, V.J., Arroyo, J., and Nombela, C. (2000). A novel family of cell wall-related proteins regulated differently during the yeast life cycle. Mol. Cell. Biol. 20, 3245-3255.
64. 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.
65. Sherman, F. (1991). Getting started with yeast. Methods Enzymol. 194, 3-20.
66. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
67. Sipos, G., Puoti, A., and Conzelmann, A. (1994). Glycosylphosphatidylinositol membrane anchors in Saccharomyces cerevisiae: absence of ceramides from complete precursor glycolipids. EMBO J. 13, 2789-2796.
68. Tabb, J.S., Molyneaux, B.J., Cohen, D.L., Kuznetsov, S.A., and Langford, G.M. (1998). Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234.
69. Vainauskas, S., Maeda, Y., Kurniawan, H., Kinoshita, T., and Menon, A.K. (2002). Structural requirements for the recruitment of Gaa1 into a functional glycosylphosphatidylinositol transamidase complex. J. Biol. Chem. 277, 30535-30542.
70. Vainauskas, S., and Menon, A.K. (2004). A conserved proline in the last transmembrane segment of Gaa1p is required for GPI recognition by GPI transamidase. J. Biol. Chem. 279, 6540-6545.
71. Wiederkehr, A., Du, Y., Pypaert, M., Ferro-Novick, S., and Novick, P. (2003). Sec3p is needed for the spatial regulation of secretion and for the inheritance of the cortical endoplasmic reticulum. Mol. Biol. Cell 14, 4770-4782.
72. Wollert, T., Weiss, D.G., Gerdes, H.H., and Kuznetsov, S.A. (2002). Activation of myosin V-based motility and F-actin-dependent network formation of endoplasmic reticulum during mitosis. J. Cell Biol. 159, 571-577.
73. Yin, H., Pruyne, D., Huffaker, T.C., and Bretscher, A. (2000). Myosin V orientates the mitotic spindle in yeast. Nature (London) 406, 1013-1015.