Mutations in proteins of the Conserved Oligomeric Golgi Complex affect polarity, cell wall structure, and glycosylation in the filamentous fungus Aspergillus nidulans

Fungal Genetics and Biology

Volumn 73, Issue , 2014, Pages 69-82

  Gremillion, S K ^a   Harris, S D ^b   Jackson Hayes, L ^c   Kaminskyj, S G W ^d   Loprete, D M ^c   Gauthier, A C ^a   Mercer, S ^c   Ravita, A J ^a   Hill, T W ^c  

^a GEORGIA SOUTHERN UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c RHODES COLLEGE   (United States)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Aspergillus nidulans; Cell wall; COG complex; Glycosylation; Polarity maintenance

Indexed keywords

FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN COG2; PROTEIN COG4; UNCLASSIFIED DRUG; CARRIER PROTEIN; COG2 PROTEIN, S CEREVISIAE; COG4 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL MIGRATION; CELL POLARITY; COG2 GENE; COG4 GENE; CONTROLLED STUDY; DOWN REGULATION; EMERICELLA NIDULANS; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS HYPHAE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCATION; GLYCOSYLATION; GOLGI COMPLEX; MUTATIONAL ANALYSIS; NONHUMAN; PODB GENE; SWOP GENE; TEMPERATURE MEASUREMENT; AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; CELL WALL; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; CELL POLARITY; CELL WALL; FUNGAL PROTEINS; GLYCOSYLATION; GOLGI APPARATUS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84908621408     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2014.10.005     Document Type: Article

References (71)

1. Breakspear A., Langford K.J., Momany M., Assinder S.J. CopA:GFP localizes to putative Golgi equivalents in Aspergillus nidulans. FEMS Microbiol Lett. 2007, 277:90-97.
2. Bruinsma P., Spelbrink R.G., Nothwehr S.F. Retrograde transport of the mannosyltransferase Och1p to the early Golgi requires a component of the COG transport complex. J. Biol. Chem. 2004, 279:39814-39823.
3. Clutterbuck A.J., Arst H. Genetic nomenclature guide: Aspergillus nidulans. Trends Genet. 1995, 11:13-14.
4. Fotso P., Koryakina Y., Pavliv O., Tsiomenko A.B., Lupashin V.V. Cog1p plays a central role in the organization of the yeast conserved oligomeric Golgi complex. J. Biol. Chem. 2005, 280:27613-27623.
5. Foulquier F. COG defects, birth and rise!. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 2009, 1792:896-902.
6. Foulquier F., Ungar D., Reynders E., Zeevaert R., Mills P., Garcia-Silva M., Briones P., Winchester B., Morelle W., Krieger M., Annaert W., Matthijs G. A new inborn error of glycosylation due to a Cog8 deficiency reveals a critical role for the Cog1-Cog8 interaction in COG complex formation. Hum. Mol. Genet. 2007, 16:717-730.
7. Fradin C., Slomianny M.C., Mille C., Masset A., Robert R., Sendid B., Ernst J.F., Michalski J.C., Poulain D. β-1,2 Oligomannose adhesin epitopes are widely distributed over the different families of Candida albicans cell wall mannoproteins and are associated through both N- and O-glycosylation processes. Infect. Immun. 2008, 76:4509-4517.
8. Guest G.M., Lin X., Momany M. Aspergillus nidulans RhoA is involved in polar growth, branching, and cell wall synthesis. Fungal Genet. Biol. 2004, 41:13-22.
9. Harris S.D. Golgi organization and the apical extension of fungal hyphae: an essential relationship. Mol. Microbiol. 2013, 89:212-215.
10. Harris S.D., Momany M. Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet. Biol. 2004, 41:391-400.
11. Harris S.D., Morrell J.L., Hamer J.E. Identification and characterization of Aspergillus nidulans Mutants defective in cytokinesis. Genetics 1994, 136:517-532.
12. Harris S.D., Hofmann A.F., Tedford H.W., Lee M.P. Identification and characterization of genes required for hyphal morphogenesis in the filamentous fungus Aspergillus nidulans. Genetics [Genetics] 1999, 151(3):1015-1025. March.
13. Harris S.D., Turner G., Meyer V., Espeso E.A., Specht T., Takeshita N., Helmstedt K. Morphology and development in Aspergillus nidulans: a complex puzzle. Fungal Genet. Biol. 2009, 46:S82-S92.
14. Hill T., Kafer E. Improved protocols for Aspergillus minimal medium: trace element and minimal medium salt stock solutions. Fungal Genet. Newslett. 2001, 48:20-21.
15. Jackson-Hayes L., Hill T.W., Loprete D.M., Fay L.M., Gordon B.S., Nkashama S.A., Patel R.K., Sartain C.V. Two GDP-mannose transporters contribute to hyphal form and cell wall integrity in Aspergillus nidulans. Microbiology 2008, 154:2037-2047.
16. Kafer E. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv. Genet. 1977, 19:33-131.
17. Kaminskyj S.G.W. Septum position is marked at the tip of Aspergillus nidulans hyphae. Fungal Genet. Biol. 2000, 31:105-113.
18. Kim D.W., Sacher M., Scarpa A., Quinn A.M., Ferro-Novick S. High-copy suppressor analysis reveals a physical interaction between Sec34p and Sec35p, a protein implicated in vesicle docking. Mol. Biol. Cell. 1999, 10:3317-3329.
19. Kim D.W., Massey T., Sacher M., Pypaert M., Ferro-Novick S. Sgf1p, a new component of the Sec34p/Sec35p Complex. Traffic 2001, 2:820-830.
20. Kingsley D.M., Kozarsky K.F., Segal M., Krieger M. Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains. J. Cell Biol. 1986, 102:1576-1585.
21. Kriangkripipat T., Momany M. Aspergillus nidulans protein O-mannosyltransferases play roles in cell wall integrity and developmental patterning. Eukaryot. Cell 2009, 8:1475-1485.
22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nat. (Lond.) 1970, 227:680-685.
23. Lee S.C., Shaw B.D. A novel interaction between N-myristoylation and the 26S proteasome during cell morphogenesis. Mol. Microbiol. 2007, 63:1039-1053.
24. Lees J.A., Yip C.K., Walz T., Hughson F.M. Molecular organization of the COG vesicle tethering complex. Nat. Struct. Mol. Biol. 2010, 17:1292-1297.
25. Levin D.E. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 2011, 189:1145-1175.
26. Liu W., May G.S., Lionakis M.S., Lewis R.E., Kontoyiannis D.P. Extra copies of the Aspergillus fumigatus squalene epoxidase gene confer resistance to terbinafine: genetic approach to studying gene dose-dependent resistance to antifungals in A. fumigatus. Antimicrob. Agents Chemother. 2004, 48:2490-2496.
27. The Fungal Genetics Stock Center: From Molds to Molecules 2003, Elsevier, New York. K. McCluskey (Ed.).
28. Miller V.J., Ungar D. Re'COG'nition at the Golgi. Traffic 2012, 13:891-897.
29. Miller V.J., Sharma P., Kudlyk T.A., Frost L., Rofe A.P., Watson I.J., Duden R., Lowe M., Lupashin V.V., Ungar D. Molecular insights into vesicle tethering at the Golgi by the conserved oligomeric Golgi (COG) complex and the Golgin TATA element modulatory factor (TMF). J. Biol. Chem. 2013, 288:4229-4240.
30. Momany M. Polarity in filamentous fungi: establishment, maintenance and new axes. Curr. Opin. Microbiol. 2002, 5:580-585.
31. Momany M., Taylor I. Landmarks in the early duplication cycles of Aspergillus fumigatus and Aspergillus nidulans: polarity, germ tube emergence and septation. Microbiology 2000, 146:3279-3284.
32. Momany M., Westfall P.J., Abramowsky G. Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics 1999, 151:557-567.
33. Oka T., Ungar D., Hughson F.M., Krieger M. The COG and COPI complexes interact to control the abundance of GEARs, a subset of Golgi integral membrane proteins. Mol. Biol. Cell 2004, 15:2423-2435.
34. Oka T., Vasile E., Penman M., Novina C.D., Dykxhoorn D.M., Ungar D., Hughson F.M., Krieger M. Genetic analysis of the subunit organization and function of the conserved oligomeric Golgi (COG) complex. J. Biol. Chem. 2005, 280:32736-32745.
35. Osherov N., May G.S. Optimization of protein extraction from Aspergillus nidulans for gel electrophoresis. Fungal Genet. Newslett. 1998, 45:38-40.
36. Osherov N., Mathew J., May G.S. Polarity-defective mutants of Aspergillus nidulans. Fungal Genet. Biol. 2000, 31:181-188.
37. Osmani A.H., Oakley B.R., Osmani S.A. Identification and analysis of essential Aspergillus nidulans genes using the heterokaryon rescue technique. Nat. Protoc. 2006, 1:2517-2526.
38. Pantazopoulou A., Peñalva M.A. Organization and dynamics of the Aspergillus nidulans Golgi during apical extension and mitosis. Mol. Biol. Cell 2009, 20:4335-4347.
39. Peanne R., Legrand D., Duvet S., Mir A.-M., Matthijs G., Rohrer J., Foulquier F. Differential effects of lobe A and lobe B of the conserved oligomeric Golgi complex on the stability of β1,4-galactosyltransferase 1 and α2,6-sialyltransferase 1. Glycobiology 2011, 21:864-876.
40. Philip B., Levin D.E. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 2001, 21:271-280.
41. Pinar M., Pantazopoulou A., Arst H.N., Peñalva M.A. Acute inactivation of the Aspergillus nidulans Golgi membrane fusion machinery: correlation of apical extension arrest and tip swelling with cisternal disorganization. Mol. Microbiol. 2013, 89:228-248.
42. Podos S.D., Reddy P., Ashkenas J., Krieger M. LDLC encodes a brefeldin A-sensitive, peripheral Golgi protein required for normal Golgi function. J. Cell Biol. 1994, 127:679-691.
43. Pokrovskaya I.D., Willett R., Smith R.D., Morelle W., Kudlyk T., Lupashin V.V. Conserved oligomeric Golgi complex specifically regulates the maintenance of Golgi glycosylation machinery. Glycobiology 2011, 21:1554-1569.
44. Rajavel M., Philip B., Buehrer B.M., Errede B., Levin D.E. Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:3969-3976.
45. Ram R.J., Li B., Kaiser C.A. Identification of Sec36p, Sec37p, and Sec38p: components of yeast complex that contains Sec34p and Sec35p. Mol. Biol. Cell. 2002, 13:1484-1500.
46. Read N.D. Exocytosis and growth do not occur only at hyphal tips. Mol. Microbiol. 2011, 81:4-7.
47. Reddy P., Krieger M. Isolation and characterization of an extragenic suppressor of the low-density lipoprotein receptor-deficient phenotype of a Chinese hamster ovary cell mutant. Mol. Cell. Biol. 1989, 9:4799-4806.
48. Romero B., Turner G., Olivas I., Laborda F., Ramón De Lucas J. The Aspergillus nidulans alcA promoter drives tightly regulated conditional gene expression in Aspergillus fumigatus permitting validation of essential genes in this human pathogen. Fungal Genet. Biol. 2003, 40:103-114.
49. Ronen R., Sharon H., Levdansky E., Romano J., Shadkchan Y., Osherov N. The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity. Curr. Genet. 2007, 51:321-329.
50. Shaw B.D., Momany M. Aspergillus nidulans polarity mutant swoA is complemented by protein O-mannosyltransferase pmtA. Fungal Genet. Biol. 2002, 37:263-270.
51. Shaw B.D., Upadhyay S. Aspergillus nidulans swoK encodes an RNA binding protein that is important for cell polarity. Fungal Genet. Biol. 2005, 42:862-872.
52. Shestakova A., Zolov S., Lupashin V. COG complex-mediated recycling of Golgi glycosyltransferases is essential for normal protein glycosylation. Traffic 2006, 7:191-204.
53. Shi X., Sha Y., Kaminskyj S. Aspergillus nidulans hypA regulates morphogenesis through the secretion pathway. Fungal Genet. Biol. 2004, 41:75-88.
54. Sohda M., Misumi Y., Yoshimura S.-I., Nakamura N., Fusano T., Ogata S., Sakisaka S., Ikehara Y. The interaction of two tethering factors, p115 and COG complex, is required for Golgi integrity. Traffic 2007, 8:270-284.
55. Spelbrink R.G., Nothwehr S.F. The yeast GRD20 gene is required for protein sorting in the trans-Golgi Network/endosomal system and for polarization of the actin cytoskeleton. Mol. Biol. Cell. 1999, 10:4263-4281.
56. Struwe W.B., Reinhold V.N. The conserved oligomeric Golgi (COG) complex is required for fucosylation of N-glycans in C. elegans. Glycobiology 2012.
57. Suvorova E.S., Duden R., Lupashin V.V. The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J. Cell Biol. 2002, 157:631-643.
58. Szewczyk E., Nayak T., Oakley C.E., Edgerton H., Xiong Y., Taheri-Talesh N., Osmani S.A., Oakley B.R. Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 2006, 1:3111-3120.
59. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. 1979, 76:4350-4354.
60. Ungar D., Oka T., Vasile E., Krieger M., Hughson F.M. Subunit architecture of the conserved oligomeric Golgi complex. J. Biol. Chem. 2005, 280:32729-32735.
61. Ungar D., Oka T., Krieger M., Hughson F.M. Retrograde transport on the COG railway. Trends Cell Biol. 2006, 16:113-120.
62. Upadhyay S., Shaw B.D. A phosphoglucose isomerase mutant in Aspergillus nidulans is defective in hyphal polarity and conidiation. Fungal Genet. Biol. 2006, 43:739-751.
63. Whyte J.R.C., Munro S. The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev. Cell 2001, 1:527-537.
64. Whyte J., Munro S. Vesicle tethering complexes in membrane traffic. J Cell Sci. 2002, 115:2627-2637.
65. Willett R., Pokrovskaya I., Lupashin V. Fluorescent microscopy as a tool to elucidate dysfunction and mislocalization of Golgi glycosyltransferases in COG complex depleted mammalian cells. Glycosyltransferases 2013, 61-72. Humana Press. I. Brockhausen (Ed.).
66. Willett R., Ungar D., Lupashin V. The Golgi puppet master: COG complex at center stage of membrane trafficking interactions. Histochem. Cell Biol. 2013, 1-13.
67. Wu X., Steet R.A., Bohorov O., Bakker J., Newell J., Krieger M., Spaapen L., Kornfeld S., Freeze H.H. Mutation of the COG complex subunit gene COG7 causes a lethal congenital disorder. Nat Med. 2004, 10:518-523.
68. Wuestehube L.J., Duden R., Eun A., Hamamoto S., Korn P., Ram R., Schekman R. New mutants of Saccharomyces cerevisiae affected in the transport of proteins from the endoplasmic reticulum to the Golgi complex. Genetics 1996, 142:393-406.
69. Yang Y., El-Ganiny A.M., Bray G.E., Sanders D.A.R., Kaminskyj S.G.W. Aspergillus nidulans hypB encodes a Sec7-domain protein important for hyphal morphogenesis. Fungal Genet. Biol. 2008, 45:749-759.
70. Yelton M.M., Hamer J.E., Timberlake W.E. Transformation of Aspergillus nidulans by using a trpC plasmid. Proc. Natl. Acad. Sci. 1984, 81:1470-1474.
71. Zolov S.N., Lupashin V.V. Cog3p depletion blocks vesicle-mediated Golgi retrograde trafficking in HeLa cells. J. Cell Biol. 2005, 168:747-759.