A bacterial glycosidase enables mannose-6-phosphate modification and improved cellular uptake of yeast-produced recombinant human lysosomal enzymes

Nature Biotechnology

Volumn 30, Issue 12, 2012, Pages 1225-1231

  Tiels, Petra ^a,b   Baranova, Ekaterina ^a,c   Piens, Kathleen ^d   De Visscher, Charlotte ^a,b   Pynaert, Gwenda ^d   Nerinckx, Wim ^a,b   Stout, Jan ^d   Fudalej, Franck ^a   Hulpiau, Paco ^d   Tännler, Simon ^d   Geysens, Steven ^d   Van Hecke, Annelies ^a,b   Valevska, Albena ^d   Vervecken, Wouter ^d   Remaut, Han ^a,c   Callewaert, Nico ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d Oxyrane   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR UPTAKE; GLUCOSIDASE; GLYCOSIDASES; LOW LEVEL; LYSOSOMAL ENZYMES; MAMMALIAN CELLS; MANNOSIDASE; MOUSE MODELS; N-GLYCANS; POMPE DISEASE; SUBSTRATE SPECIFICITY;

CELL CULTURE; MAMMALS; YEAST;

ENZYMES;

ALPHA GLUCOSIDASE; ALPHA MANNOSIDASE; GLYCAN DERIVATIVE; GLYCOSIDASE; LYSOSOME ENZYME; MANNOSE 6 PHOSPHATE; N GLYCAN DERIVATIVE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM; CELLULOSIMICROBIUM CELLULANS; ENZYME STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; YEAST;

ALPHA-GLUCOSIDASES; ANIMALS; ARTHROBACTER; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; BIOTECHNOLOGY; CATALYTIC DOMAIN; DISEASE MODELS, ANIMAL; GLYCOGEN STORAGE DISEASE TYPE II; GLYCOSIDE HYDROLASES; HUMANS; LYSOSOMAL STORAGE DISEASES; LYSOSOMES; MANNOSEPHOSPHATES; MICE; MICE, KNOCKOUT; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PICHIA; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; YARROWIA;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 84870946443     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2427     Document Type: Article

References (41)

1. Futerman, A.H. & van Meer, G. The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol. 5, 554-565 (2004).
2. Desnick, R.J. & Schuchman, E.H. Enzyme replacement and enhancement therapies: lessons from lysosomal disorders. Nat. Rev. Genet. 3, 954-966 (2002).
3. Pohl, S., Marschner, K., Storch, S. & Braulke, T. Glycosylation- and phosphorylation-dependent intracellular transport of lysosomal hydrolases. Biol. Chem. 390, 521-527 (2009).
4. Dahms, N.M., Lobel, P. & Kornfeld, S. Mannose 6-phosphate receptors and lysosomal enzyme targeting. J. Biol. Chem. 264, 12115-12118 (1989).
5. Hille-Rehfeld, A. Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta 1241, 177-194 (1995).
6. Chiba, Y. et al. Production in yeast of α-galactosidase A, a lysosomal enzyme applicable to enzyme replacement therapy for Fabry disease. Glycobiology 12, 821-828 (2002).
7. Braulke, T., Gartung, C., Hasilik, A. & von Figura, K. Is movement of mannose 6-phosphate-specific receptor triggered by binding of lysosomal enzymes? J. Cell Biol. 104, 1735-1742 (1987).
8. Dahms, N.M. & Hancock, M.K. P-type lectins. Biochim. Biophys. Acta 1572, 317-340 (2002).
9. Breuer, P. et al. Serine phosphorylation site of the 46-kDa mannose 6-phosphate receptor is required for transport to the plasma membrane in Madin-Darby canine kidney and mouse fibroblast cells. Mol. Biol. Cell 8, 567-576 (1997).
10. Beck, M. New therapeutic options for lysosomal storage disorders: enzyme replacement, small molecules and gene therapy. Hum. Genet. 121, 1-22 (2007).
11. Zhu, Y. et al. Carbohydrate-remodelled acid α-glucosidase with higher affinity for the cation-independent mannose 6-phosphate receptor demonstrates improved delivery to muscles of Pompe mice. Biochem. J. 389, 619-628 (2005).
12. Odani, T., Shimma, Y., Tanaka, A. & Jigami, Y. Cloning and analysis of the MNN4 gene required for phosphorylation of N-linked oligosaccharides in Saccharomyces cerevisiae. Glycobiology 6, 805-810 (1996).
13. Jigami, Y. & Odani, T. Mannosylphosphate transfer to yeast mannan. Biochim. Biophys. Acta 1426, 335-345 (1999).
14. Ballou, D.L. Genetic control of yeast mannan structure: mapping genes mnn2 and mnn4 in Saccharomyces cerevisiae. J. Bacteriol. 123, 616-619 (1975).
15. Akeboshi, H. et al. Production of human β-hexosaminidase A with highly phosphorylated N-glycans by the overexpression of the Ogataea minuta MNN4 gene. Glycobiology 19, 1002-1009 (2009).
16. York, S.J., Arneson, L.S., Gregory, W.T., Dahms, N.M. & Kornfeld, S. The Rate of Internalization of the mannose 6-phosphate/insulin-like growth factor II receptor is enhanced by multivalent ligand binding. J. Biol. Chem. 274, 1164-1171 (1999).
17. Struhl, K., Stinchcomb, D.T., Scherer, S. & Davis, R.W. High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules. Proc. Natl. Acad. Sci. USA 76, 1035-1039 (1979).
18. Scott, J.H. & Schekman, R. Lyticase: endoglucanase and protease activities that act together in yeast cell lysis. J. Bacteriol. 142, 414-423 (1980).
19. Schwientek, P., Szczepanowski, R., Rückert, C., Stoye, J. & Pühler, A. Sequencing of high G +°C microbial genomes using the ultrafast pyrosequencing technology. J. Biotechnol. 155, 68-77 (2011).
20. Laroy, W., Contreras, R. & Callewaert, N. Glycome mapping on DNA sequencing equipment. Nat. Protoc. 1, 397-405 (2006).
21. Takashiba, M., Chiba, Y. & Jigami, Y. Identification of phosphorylation sites in N-linked glycans by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Chem. 78, 5208-5213 (2006).
22. Zhu, Y. et al. Mechanistic insights into a Ca2+-dependent family of alpha-mannosidases in a human gut symbiont. Nat. Chem. Biol. 6, 125-132 (2010).
23. Lee, K. et al. A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease. Glycobiology 13, 305-313 (2003).
24. Bijvoet, A.G. et al. Generalized glycogen storage and cardiomegaly in a knockout mouse model of Pompe disease. Hum. Mol. Genet. 7, 53-62 (1998).
25. Zhu, Y. et al. Glycoengineered acid alpha-glucosidase with improved efficacy at correcting the metabolic aberrations and motor function deficits in a mouse model of Pompe disease. Mol. Ther. 17, 954-963 (2009).
26. Metcalfe, G. & Brown, M.E. Nitrogen fixation by new species of Nocardia. J. Gen. Microbiol. 17, 567-572 (1957).
27. Schumann, P., Weiss, N. & Stackebrandt, E. Reclassification of Cellulomonas cellulans (Stackebrandt and Keddie 1986) as Cellulosimicrobium cellulans gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 51, 1007-1010 (2001).
28. Fickers, P. et al. Identification and characterisation of LIP7 and LIP8 genes encoding two extracellular triacylglycerol lipases in the yeast Yarrowia lipolytica. Fungal Genet. Biol. 42, 264-274 (2005).
29. De Pourcq, K. et al. Engineering the yeast Yarrowia lipolytica for the production of therapeutic proteins homogeneously glycosylated with Man8GlcNAc2 and Man5GlcNAc2. Microb. Cell Fact. 11, 53 (2012).
30. Vervecken, W. et al. In vivo synthesis of mammalian-like, hybrid-type N-glycans in Pichia pastoris. Appl. Environ. Microbiol. 70, 2639-2646 (2004).
31. Barth, G. & Gaillardin, C. Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol. Rev. 19, 219-237 (1997).
32. Fickers, P., Le Dall, M.T., Gaillardin, C., Thonart, P. & Nicaud, J.M. New disruption cassettes for rapid gene disruption and marker rescue in the yeast Yarrowia lipolytica. J. Microbiol. Methods 55, 727-737 (2003).
33. Miura, M., Hirose, M., Miwa, T., Kuwae, S. & Ohi, H. Cloning and characterization in Pichia pastoris of PNO1 gene required for phosphomannosylation of N-linked oligosaccharides. Gene 324, 129-137 (2004).
34. Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr. 66, 133-144 (2010).
35. Terwilliger, T.C. et al. Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr. 65, 582-601 (2009).
36. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
37. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
38. Halgren, T.A. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J. Comput. Chem. 17, 490-519 (1996).
39. Morris, G.M. et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791 (2009).
40. Trott, O. & Olson, A.J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461 (2010).
41. Reuser, A.J. et al. Uptake and stability of human and bovine acid alpha-glucosidase in cultured fibroblasts and skeletal muscle cells from glycogenosis type II patients. Exp. Cell Res. 155, 178-189 (1984).