Cloning and functional analysis of the dpm2 and dpm3 genes from Trichoderma reesei expressed in a Saccharomyces cerevisiae dpm1Δ mutant strain

Biological Chemistry

Volumn 392, Issue 6, 2011, Pages 517-527

  Zembek, Patrycja ^a   Perlińska Lenart, Urszula ^a   Rawa, Katarzyna ^a   Górka Nieć, Wioletta ^a   Palamarczyk, Grazyna ^a   Kruszewska, Joanna S ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

cell wall composition; DPM synthase; O glycosylation; Trichoderma reesei

Indexed keywords

DOLICHOL PHOSPHATE MANNOSE; DOLICHOL PHOSPHATE MANNOSE 1; DOLICHOL PHOSPHATE MANNOSE 2; DOLICHOL PHOSPHATE MANNOSE 3; MANNOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL WALL; ENZYME ANALYSIS; FUNGAL STRAIN; GLYCOSYLATION; HYPOCREA JECORINA; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

CLONING, MOLECULAR; GENE EXPRESSION; GENOTYPE; MANNOSYLTRANSFERASES; MUTATION; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; TRICHODERMA;

HYPOCREA JECORINA; SACCHAROMYCES CEREVISIAE;

EID: 79958071043     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2011.058     Document Type: Article

References (49)

1. Agaphonov, M.O., Packeiser, A.N., Chechenova, M.B., Choi, E., and Ter-Avanesyan, M.D. (2001). Mutation of the homologue of GDP-mannose pyrophosphorylase alters cell wall structure, protein glycosylation and secretion in Hansenula polymorpha. Yeast 18, 391-402. (Pubitemid 32266191)
2. Agaphonov, M.O., Sokolov, S., Romanova, N.V., Sohn, J., Kim, S.Y., Kalebina, T.S., Choi, E.S., and Ter-Avanesyan, M.D. (2005). Mutation of the protein-O-mannosyltransferase enhances secretion of the human urokinase-type plasminogen activator in Hansenula polymorpha. Yeast 22, 1037-1047. (Pubitemid 41582365)
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. (Pubitemid 27359211)
4. Arroyo-Flores, B.L., Calvo-Mendez, C., Flores-Carreon, A., and Lopez-Romero, E. (2005). Biosynthesis of glycoproteins in the pathogenic fungus Candida albicans: activation of dolichol phosphate mannose synthase by cAMP-mediated protein phosphorylation. FEMS Immunol. Med. Microbiol. 45, 429-434. (Pubitemid 41247779)
5. Ashida, H., Maeda, Y., and Kinoshita, T. (2006). DPM1, the catalytic subunit of dolichol-phosphate mannose synthase, is tethered to and stabilized on the endoplasmic reticulum membrane by DPM3. J. Biol. Chem. 281, 896-904.
6. Banerjee, D.K., Kousvelari, E.E., and Baum, B.J. (1987). c-AMP mediated protein phosphorylation microsomal membranes increases mannosylphosphodolichol synthase activity. Proc. Natl. Acad. Sci. USA 84, 6389-6393.
7. Banerjee, D.K., Carrasquillo, E.A., Hughey, P., Schutzbach, J.S., Martinez, J.A., and Baksi, K. (2005). In vitro phosphorylation by cAMP-dependent protein kinase up-regulates recombinant Saccharomyces cerevisiae mannosylphosphodolichol synthase. J. Biol. Chem. 280, 4174-4181. (Pubitemid 40288582)
8. Chen, D., Yang, B., and Kuo, T. (1992). One-step transformation of yeast in stationary phase. Curr. Genet. 21, 83-84.
9. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinum thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159. (Pubitemid 17064313)
10. Colussi, P.A., Taron, C.H., Mach, J.C., and Orlean, P. (1997). Human and Saccharomyces cerevisiae dolichol phosphate mannose synthases represent two classes of the enzyme, but both function in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 94, 7873-7878. (Pubitemid 27343742)
11. Doucey, M., Hess, D., Cacan, R., and Hofsteenge, J. (1998). Protein C-mannosylation is enzyme-catalysed and uses dolichyl-phosphate- mannose as a precursor. Mol. Biol. Cell 9, 291-300. (Pubitemid 28084125)
12. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., et al. (2011). Geneious v5.4. Available from http://www.geneious.com/.
13. Herscovics, A. and Orlean, P. (1993). Glycoprotein synthesis in yeast. FASEB J. 7, 540-550.
14. Hoffman, C.S. and Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57, 267-272. (Pubitemid 18007116)
15. Hofmann, K. and Stoffel, W. (1993). TMbase - a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 374, 166.
16. Imbach, T., Schenk, B., Schollen, E., Burda, P., Stutz, A., Grünewald, S., Bailie, N.M., King, M.D., Jaeken, J., Matthijs, G. et al. (2000). Deficiency of dolichol-phosphate-mannose synthase- 1causes congenital disorder of glycosylation type Ie. J. Clin. Invest. 105, 233-239. (Pubitemid 30054363)
17. Immervoll, T., Gentzsch, M., and Tanner, W. (1995). PMT3 and PMT4, two new members of the protein-O-mannosyltransferase gene family of Saccharomyces cerevisiae. Yeast 11, 1345-1351.
18. Janik, A., Sosnowska, M., Kruszewska, J., Krotkiewski, H., Lehle, L., and Palamarczyk, G. (2003). Overexpression of GDP-mannose pyrophosphorylase in Saccharomyces cerevisiae corrects defects in dolichol-linked saccharide formation and protein glycosylation. Biochim. Biophys. Acta 1621, 22-30. (Pubitemid 36349694)
19. Jukes, T.H. and Cantor, C.R. (1969). Evolution of protein molecules. In: Mammalian protein metabolism. H.N. Munro, ed. (New York: Academic Press), pp. 21-123.
20. Kim, S., Westphal, V., Srikrishna, G., Mehta, D.P., Peterson, S., Filiano, J., Karnes, P.S., Patterson, M.C., and Freeze, H.H. (2000). Dolichol phosphate mannose synthase (DPM1) mutations define congenital disorder of glycosylation Ie (CDG-Ie) J. Clin. Invest. 105, 191-198. (Pubitemid 30054358)
21. Kim, M.W., Kim, E.J., Kim, J., Park, J., Oh, D., Shimma, Y., Chiba, Y., Jigami, Y., Rhee, S.K., and Kang, H.A. (2006). Functional characterization of the Hansenula polymorpha HOC1, OCH1, and OCR1 genes as members of the yeast OCH1 mannosyltransferase family involved in protein glycosylation. J. Biol. Chem. 281, 6261-6272. (Pubitemid 43847557)
22. Kruszewska, J., Messner, R., Kubicek, C.P., and Palamarczyk, G. (1989). O-glycosylation of proteins by membrane fraction of Trichoderma reesei QM9414. J. Gen. Microbiol. 135, 301-307. (Pubitemid 19062474)
23. Kruszewska, J., Palamarczyk, G., and Kubicek, C.P. (1991). Mannosyl phosphodolichol synthase is activated by protein kinase dependent phosphorylation in vitro. FEMS Lett. 80, 81-86.
24. Kruszewska, J., Butterweck, A.H., Kurzatkowski,W., Migdalski, A., Kubicek, C.P., and Palamarczyk, G. (1999). Overexpression of the Saccharomyces cerevisiae mannosylphosphodolichol synthase encoding gene in Trichoderma reesei results in an increased level of protein secretion and abnormal cell ultrastructure. Appl. Environm. Microbiol. 65, 2382-2387.
25. Kruszewska, J.S., Saloheimo, M., Migdalski, A., Orlean, P., Penttila, M., and Palamarczyk, G. (2000). Dolichol phosphate mannose synthase from the filamentous fungus Trichoderma reesei belongs to the human and Schizosaccharomyces pombe class of the enzyme. Glycobiology 10, 983-991.
26. Kuranda, M.J. and Robins, P.W. (1991). Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J. Biol. Chem. 266, 19758-19767. (Pubitemid 21908292)
27. Lefeber, D.J., Schonberger, J., Morava, E., Guillard, M., Huyben, K.M., Verrijp, K., Grafakou, O., Evangeliou, A., Preijers, F.W., Manta, P. et al. (2009). Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am. J. Hum. Genet. 85, 76-86.
28. Lommel, M., Bognat, M., and Strahl, S. (2004). Aberrant processing of the WSC family and Mid2p cell surface sensors in cell death of Saccharomyces cerevisiae O-mannosylation mutants. Mol. Cell. Biol. 24, 46-57. (Pubitemid 38010034)
29. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
30. Maeda, Y. and Kinoshita, T. (2008). Dolichol-phosphate mannose synthase: structure, function and regulation. Biochim. Biophys. Acta 1780, 861-868.
31. Maeda, Y., Tomita, S., Watanabe, R., Ohishi, K., and Kinoshita, T. (1998). DPM2 regulates biosynhesis of dolichol phosphate mannose in mammalian cells: correct subcellular localization and stabilization of DPM1 and binding of dolichol phosphate. EMBO J. 17, 4920-4929. (Pubitemid 28408459)
32. Maeda, Y., Tanaka, S., Hino, J., Kangawa, K., and Kinoshita, T. (2000). Human dolichol-phosphate-mannose synthase consists of three subunits, DPM1, DPM2 and DPM3. EMBO J. 11, 2475-2482. (Pubitemid 30323537)
33. Miller, G.L., Blum, R., Glennon, W.E., and Burton, A.L. (1960). Measurements of carboxymethylcellulase activity. Anal. Biochem. 2, 127-132.
34. Munberg, D., Muller, R., and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119-122.
35. Orlean, P., Albright, C.F., and Robbins, P.W. (1988). Cloning and sequencing of the yeast gene for dolichol phosphate mannose synthase, an essential protein. J. Biol. Chem. 263, 17499-17507.
36. Orlean, P. (1990). Dolichol phosphate mannose synthase is required in vivo for glycosyl phosphatidylinositol membrane anchoring, O Mannosylation, and N glycosylation of protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 5796-5805.
37. Orlean, P. (1992). Enzymes that recognize dolichols participate in three glycosylation pathways and are required for protein secretion. Biochem. Cell. Biol. 70, 438-447.
38. Orłlowski, J., Machułla, K., Janik, A., Zdebska, E., and Palamarczyk, G. (2007). Dissecting the role of dolichol in cell wall assembly in the yeast mutants impaired in early glycosylation reactions. Yeast 24, 239-252. (Pubitemid 46696280)
39. Perlińska-Lenart, U., Kurzatkowski, W., Janas, P., Kopińska, A., Palamarczyk, G., and Kruszewska, J.S. (2005). Protein production and secretion in an Aspergillus nidulans mutant impaired in glycosylation. Acta Biochim. Pol. 52, 195-205. (Pubitemid 41132187)
40. Perlińska-Lenart, U., Orłlowski, J., Laudy, A.E., Zdebska, E., Palamarczyk, G., and Kruszewska, J.S. (2006). Glycoprotein hypersecretion alters the cell wall in Trichoderma reesei strains expressing the Saccharomyces cerevisiae dolichylphosphate mannose synthase gene. Appl. Environ. Microbiol. 72, 7778-7784. (Pubitemid 44927684)
41. Reissig, J.L., Storminger, J.L., and Leloir, L.F. (1955). A modified colorimetric method for the estimation of N-acetylamino sugars. J. Biol. Chem. 217, 959-966.
42. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning: a laboratory manual. 2nd Edition. Vol. 1 (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press), pp. 7.37-7.52.
43. Sharma, C.B., Babczinski, P., Lehle, L., and Tanner, W. (1974). The role of dolicholmonophosphate in glycoprotein biosynthesis in Saccharomyces cerevisiae. Eur. J. Biochem. 46, 35-41.
44. Sherman, F. (1991). Getting started with yeast. In: Guide to Yeast Genetics and Molecular Biology, Methods Enzymol Vol. 194, C. Gutherie and G.R. Fink, eds. pp. 3-21.
45. Sneath, P.H.A. and Sokal, R.R. (1973). Numerical Taxonomy. (San Francisco: W.H. Freeman and Company), pp. 230-234.
46. Strahl-Bolsinger, S., Gentzsch, M., and Tanner, W. (1999). Protein O-mannosylation. Biochim. Biophys. Acta 1426, 297-307. (Pubitemid 29027946)
47. Tomita, S., Inoue, N., Maeda, Y., Ohishi, K., Takeda, J., and Kinoshita, T. (1998). A homologue of Saccharomyces cerevisiae Dpm1-p is not sufficient for synthesis of dolichol-phosphatemannose in mammalian cells. J. Biol. Chem. 273, 9249-9254. (Pubitemid 28176217)
48. Yanish-Perron, C., Vieira, J., and Messing, J. (1985). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC 19 vectors. Gene 33, 103-119. (Pubitemid 15122816)
49. Zakrzewska, A., Migdalski, A., Saloheimo, M., Penttila, M.E., Palamarczyk, G., and Kruszewska, J.S. (2003). cDNA encoding protein O-mannosyltransferase from the filamentous fungus Trichoderma reesei; functional equivalence to Saccharomyces cerevisiae PMT2. Curr. Genet. 43, 11-16. (Pubitemid 36747771)