Production of glycosylated soluble amyloid precursor protein alpha (sAPPalpha) in leishmania tarentolae

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 396-403

  Klatt, Stephan ^a,b   Rohe, Michael ^c   Alagesan, Kathirvel ^d   Kolarich, Daniel ^d   Konthur, Zoltän ^a   Hartl, Daniela ^e  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Alzheimer's disease; Amyloid precursor protein alpha; Leishmania tarentolae; PGC LC ESI MS MS N glycan analysis

Indexed keywords

AMYLOID PRECURSOR PROTEIN; HEXOSAMINE; HYDRONIUM ION; PENTASACCHARIDE; RECOMBINANT PROTEIN; SOLUBLE AMYLOID PRECURSOR PROTEIN ALPHA; UNCLASSIFIED DRUG;

ARTICLE; ENZYMATIC DEGRADATION; FRAGMENTATION REACTION; GENE EXPRESSION SYSTEM; LEISHMANIA TARENTOLAE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STABILITY;

ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; ESCHERICHIA COLI; GENE EXPRESSION; GLYCOSYLATION; HUMANS; LEISHMANIA; MASS SPECTROMETRY; PEPTIDE FRAGMENTS; RECOMBINANT PROTEINS; TANDEM MASS SPECTROMETRY;

EID: 84874046118     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300693f     Document Type: Article

References (48)

1. Sorensen, H. P.; Mortensen, K. K. Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact. 2005, 4 (1), 1.
2. Villaverde, A.; Carrio, M. M. Protein aggregation in recombinant bacteria: Biological role of inclusion bodies. Biotechnol. Lett. 2003, 25 (17), 1385-1395.
3. Konthur, Z.; Hust, M.; Dubel, S. Perspectives for systematic in vitro antibody generation. Gene 2005, 364, 19-29.
4. Kushnir, S.; Gase, K.; Breitling, R.; Alexandrov, K. Development of an inducible protein expression system based on the protozoan host Leishmania tarentolae. Protein Expression Purif. 2005, 42 (1), 37-46.
5. Mureev, S.; Kushnir, S.; Kolesnikov, A. A.; Breitling, R.; Alexandrov, K. Construction and analysis of Leishmania tarentolae transgenic strains free of selection markers. Mol. Biochem. Parasitol. 2007, 155 (2), 71-83.
6. Fritsche, C.; Sitz, M.; Weiland, N.; Breitling, R.; Pohl, H. D. Characterization of the growth behavior of Leishmania tarentolae: A new expression system for recombinant proteins. J. Basic Microbiol. 2007, 47 (5), 384-393.
7. Fritsche, C.; Sitz, M.; Wolf, M.; Pohl, H. D. Development of a defined medium for heterologous expression in Leishmania tarentolae. J. Basic Microbiol. 2008, 48 (6), 488-495.
8. La Flamme, A. C.; Buckner, F. S.; Swindle, J.; Ajioka, J.; Van Voorhis, W. C. Expression of mammalian cytokines by Trypanosoma cruzi indicates unique signal sequence requirements and processing. Mol. Biochem. Parasitol. 1995, 75 (1), 25-31.
9. Zhang, W. W.; Charest, H.; Matlashewski, G. The expression of biologically active human p53 in Leishmania cells: A novel eukaryotic system to produce recombinant proteins. Nucleic Acids Res. 1995, 23 (20), 4073-4080.
10. Breitling, R.; Klingner, S.; Callewaert, N.; Pietrucha, R.; Geyer, A.; Ehrlich, G.; Hartung, R.; Muller, A.; Contreras, R.; Beverley, S. M.; Alexandrov, K. Non-pathogenic trypanosomatid protozoa as a platform for protein research and production. Protein Expression Purif. 2002, 25 (2), 209-218.
11. Basile, G.; Peticca, M. Recombinant protein expression in Leishmania tarentolae. Mol. Biotechnol. 2009, 43 (3), 273-278.
12. Lazarov, O.; Demars, M. P. All in the Family: How the APPs Regulate Neurogenesis. Front. Neurosci. 2012, 6, 81.
13. Hartl, D.; Rohe, M.; Mao, L.; Staufenbiel, M.; Zabel, C.; Klose, J. Impairment of adolescent hippocampal plasticity in a mouse model for Alzheimer's disease precedes disease phenotype. PLoS One 2008, 3 (7), e2759.
14. Hartl, D.; Schuldt, V.; Forler, S.; Zabel, C.; Klose, J.; Rohe, M. Presymptomatic Alterations in Energy Metabolism and Oxidative Stress in the APP23 Mouse Model of Alzheimer Disease. J. Proteome Res. 2012, 11, 3295-3304.
15. Huang, Y.; Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148 (6), 1204-1222.
16. Steinacker, P.; Fang, L.; Kuhle, J.; Petzold, A.; Tumani, H.; Ludolph, A. C.; Otto, M.; Brettschneider, J. Soluble beta-amyloid precursor protein is related to disease progression in amyotrophic lateral sclerosis. PLoS One 2011, 6 (8), e23600.
17. Ray, B.; Long, J. M.; Sokol, D. K.; Lahiri, D. K. Increased secreted amyloid precursor protein-alpha (sAPPalpha) in severe autism: Proposal of a specific, anabolic pathway and putative biomarker. PLoS One 2011, 6 (6), e20405.
18. Perneczky, R.; Tsolakidou, A.; Arnold, A.; Diehl-Schmid, J.; Grimmer, T.; Forstl, H.; Kurz, A.; Alexopoulos, P. CSF solubleamyloid precursor proteins in the diagnosis of incipient Alzheimer disease. Neurology 2011, 77 (1), 35-38.
19. Wu, G.; Sankaranarayanan, S.; Hsieh, S. H.; Simon, A. J.; Savage, M. J. Decrease in brain soluble amyloid precursor protein beta (sAPPbeta) in Alzheimer's disease cortex. J. Neurosci. Res. 2011, 89 (6), 822-832.
20. Sennvik, K.; Fastbom, J.; Blomberg, M.; Wahlund, L. O.; Winblad, B.; Benedikz, E. Levels of alpha-and beta-secretase cleaved amyloid precursor protein in the cerebrospinal fluid of Alzheimer's disease patients. Neurosci. Lett. 2000, 278 (3), 169-172.
21. Mattson, M. P.; Cheng, B.; Culwell, A. R.; Esch, F. S.; Lieberburg, I.; Rydel, R. E. Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the betaamyloid precursor protein. Neuron 1993, 10 (2), 243-254.
22. Meziane, H.; Dodart, J. C.; Mathis, C.; Little, S.; Clemens, J.; Paul, S. M.; Ungerer, A. Memory-enhancing effects of secreted forms of the beta-amyloid precursor protein in normal and amnestic mice. Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (21), 12683-12688.
23. Postina, R.; Schroeder, A.; Dewachter, I.; Bohl, J.; Schmitt, U.; Kojro, E.; Prinzen, C.; Endres, K.; Hiemke, C.; Blessing, M.; Flamez, P.; Dequenne, A.; Godaux, E.; van Leuven, F.; Fahrenholz, F. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 2004, 113 (10), 1456-1464.
24. Stein, T. D.; Anders, N. J.; DeCarli, C.; Chan, S. L.; Mattson, M. P.; Johnson, J. A. Neutralization of transthyretin reverses the neuroprotective effects of secreted amyloid precursor protein (APP) in APPSW mice resulting in tau phosphorylation and loss of hippocampal neurons: support for the amyloid hypothesis. J. Neurosci. 2004, 24 (35), 7707-7717.
25. Bell, K. F.; Zheng, L.; Fahrenholz, F.; Cuello, A. C. ADAM-10 over-expression increases cortical synaptogenesis. Neurobiol. Aging 2008, 29 (4), 554-565.
26. Klatt, S.; Konthur, Z. Secretory signal peptide modification for optimized antibody-fragment expression-secretion in Leishmania tarentolae. Microbial Cell Factories 2012, 11 (97), DOI: 10.1186/1475-2859-11-97.
27. Rohe, M.; Nebrich, G.; Klein, O.; Mao, L.; Zabel, C.; Klose, J.; Hartl, D. Kainate promotes alterations in neuronal RNA splicing machinery. J. Proteome Res. 2011, 10 (4), 1459-1467.
28. Kolarich, D.; Jensen, P. H.; Altmann, F.; Packer, N. H. Determination of site-specific glycan heterogeneity on glycoproteins. Nat. Protoc. 2012, 7 (7), 1285-1298.
29. Jensen, P. H.; Karlsson, N. G.; Kolarich, D.; Packer, N. H. Structural analysis of N-and O-glycans released from glycoproteins. Nat. Protoc. 2012, 7 (7), 1299-1310.
30. Borrero, J.; Jimenez, J. J.; Gutiez, L.; Herranz, C.; Cintas, L. M.; Hernandez, P. E. Protein expression vector and secretion signal peptide optimization to drive the production, secretion, and functional expression of the bacteriocin enterocin A in lactic acid bacteria. J. Biotechnol. 2011, 156 (1), 76-86.
31. Futatsumori-Sugai, M.; Tsumoto, K. Signal peptide design for improving recombinant protein secretion in the baculovirus expression vector system. Biochem. Biophys. Res. Commun. 2010, 391 (1), 931-935.
32. Palomares, L. A.; Estrada-Mondaca, S.; Ramirez, O. T. Production of recombinant proteins: Challenges and solutions. Methods Mol. Biol. 2004, 267, 15-52.
33. Emanuelsson, O.; Brunak, S.; von Heijne, G.; Nielsen, H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2 (4), 953-971.
34. Choo, K. H.; Tan, T. W.; Ranganathan, S. A comprehensive assessment of N-terminal signal peptides prediction methods. BMC Bioinf. 2009, 10 (Suppl. 15), S2.
35. Petersen, T. N.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8 (10), 785-786.
36. Cappai, R.; Mok, S. S.; Galatis, D.; Tucker, D. F.; Henry, A.; Beyreuther, K.; Small, D. H.; Masters, C. L. Recombinant human amyloid precursor-like protein 2 (APLP2) expressed in the yeast Pichia pastoris can stimulate neurite outgrowth. FEBS Lett. 1999, 442 (1), 95-98.
37. Turner, P. R.; Bourne, K.; Garama, D.; Carne, A.; Abraham, W. C.; Tate, W. P. Production, purification and functional validation of human secreted amyloid precursor proteins for use as neuropharmacological reagents. J. Neurosci. Methods 2007, 164 (1), 68-74.
38. Rohe, M.; Carlo, A. S.; Breyhan, H.; Sporbert, A.; Militz, D.; Schmidt, V.; Wozny, C.; Harmeier, A.; Erdmann, B.; Bales, K. R.; Wolf, S.; Kempermann, G.; Paul, S. M.; Schmitz, D.; Bayer, T. A.; Willnow, T. E.; Andersen, O. M. Sortilin-related receptor with A-type repeats (SORLA) affects the amyloid precursor protein-dependent stimulation of ERK signaling and adult neurogenesis. J. Biol. Chem. 2008, 283 (21), 14826-14834.
39. Pahlsson, P.; Shakin-Eshleman, S. H.; Spitalnik, S. L. N-linked glycosylation of beta-amyloid precursor protein. Biochem. Biophys. Res. Commun. 1992, 189 (3), 1667-1673.
40. Tomita, S.; Kirino, Y.; Suzuki, T. Cleavage of Alzheimer's amyloid precursor protein (APP) by secretases occurs after Oglycosylation of APP in the protein secretory pathway. Identification of intracellular compartments in which APP cleavage occurs without using toxic agents that interfere with protein metabolism. J. Biol. Chem. 1998, 273 (11), 6277-6284.
41. Perdivara, I.; Petrovich, R.; Allinquant, B.; Deterding, L. J.; Tomer, K. B.; Przybylski, M. Elucidation of O-glycosylation structures of the beta-amyloid precursor protein by liquid chromatography-mass spectrometry using electron transfer dissociation and collision induced dissociation. J. Proteome Res. 2009, 8 (2), 631-642.
42. Georgopoulou, N.; McLaughlin, M.; McFarlane, I.; Breen, K. C. The role of post-translational modification in beta-amyloid precursor protein processing. Biochem. Soc. Symp. 2001, 67, 23-36.
43. Sola, R. J.; Griebenow, K. Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci. 2009, 98 (4), 1223-1245.
44. Gakhar-Koppole, N.; Hundeshagen, P.; Mandl, C.; Weyer, S. W.; Allinquant, B.; Muller, U.; Ciccolini, F. Activity requires soluble amyloid precursor protein alpha to promote neurite outgrowth in neural stem cell-derived neurons via activation of the MAPK pathway. Eur. J. Neurosci. 2008, 28 (5), 871-882.
45. Halim, A.; Brinkmalm, G.; Ruetschi, U.; Westman-Brinkmalm, A.; Portelius, E.; Zetterberg, H.; Blennow, K.; Larson, G.; Nilsson, J. Site-specific characterization of threonine, serine, and tyrosine glycosylations of amyloid precursor protein/amyloid beta-peptides in human cerebrospinal fluid. Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (29), 11848-11853.
46. Liu, T.; Qian, W. J.; Gritsenko, M. A.; Camp, D. G., 2nd; Monroe, M. E.; Moore, R. J.; Smith, R. D. Human plasma Nglycoproteome analysis by immunoaffinity subtraction, hydrazide chemistry, and mass spectrometry. J. Proteome Res. 2005, 4 (6), 2070-2080.
47. Parodi, A. J. Biosynthesis of protein-linked oligosaccharides in trypanosomatid flagellates. Parasitol. Today 1993, 9 (10), 373-377.
48. Mellquist, J. L.; Kasturi, L.; Spitalnik, S. L.; Shakin-Eshleman, S. H. The amino acid following an asn-X-Ser/Thr sequon is an important determinant of N-linked core glycosylation efficiency. Biochemistry 1998, 37 (19), 6833-6837.