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Glyco-Engineering Plants to Produce Helminth Glycoproteins as Prospective Biopharmaceuticals: Recent Advances, Challenges and Future Prospects

van der Kaaij, Alex, van Noort, Kim, Nibbering, Pieter, Wilbers, Ruud H. P., Schots, Arjen·2022·Frontiers in Plant Science
DOI 10.3389/fpls.2022.882835PMC PMC9100689
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Abstract

Glycoproteins are the dominant category among approved biopharmaceuticals, indicating their importance as therapeutic proteins. Glycoproteins are decorated with carbohydrate structures (or glycans) in a process called glycosylation. Glycosylation is a post-translational modification that is present in all kingdoms of life, albeit with differences in core modifications, terminal glycan structures, and incorporation of different sugar residues. Glycans play pivotal roles in many biological processes and can impact the efficacy of therapeutic glycoproteins. The majority of biopharmaceuticals are based on human glycoproteins, but non-human glycoproteins, originating from for instance parasitic worms (helminths), form an untapped pool of potential therapeutics for immune-related diseases and vaccine candidates. The production of sufficient quantities of correctly glycosylated putative therapeutic helminth proteins is often challenging and requires extensive engineering of the glycosylation pathway. Therefore, a flexible glycoprotein production system is required that allows straightforward introduction of heterologous glycosylation machinery composed of glycosyltransferases and glycosidases to obtain desired glycan structures. The glycome of plants creates an ideal starting point for N- and O-glyco-engineering of helminth glycans. Plants are also tolerant toward the introduction of heterologous glycosylation enzymes as well as the obtained glycans. Thus, a potent production platform emerges that enables the production of recombinant helminth proteins with unusual glycans. In this review, we discuss recent advances in plant glyco-engineering of potentially therapeutic helminth glycoproteins, challenges and their future prospects.

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FIGURE 1 Glycosylation pathways in plants. A schematic overview of successive glycan modifying steps in the plant secretory pathway. Glycoproteins receive an N-glycan in the endoplasmic reticulum (ER) on an asparagine residue (N) within the consensus sequence (N-X-S/T), where X can be any amino acid except proline. After ER quality control, the correctly folded protein passes through the Golgi compartment. Within the Golgi immature high mannose-type N-glycans are modified in a tightly regulated process. First, Golgi α-mannosidase I (MNS1) trims down the N-glycan to a Man5 structure. In subsequent steps a diantennary N-glycan is synthesized, which in plants is substituted with core α1,3-fucose and β1,2-xylose. In some cases [as indicated by an asterisk (*)], this N-glycan is further extended with Lewis A motifs. Once secreted into the extracellular space (or apoplast) a terminal GlcNAc glycan structure can be trimmed down to a paucimannosidic glycan by the β-hexosaminidase HEXO3. Classical O-glycan synthesis in plants is initiated by the hydroxylation of proline residues by prolyl-4-hydroxylases (P4H) in the ER and/or Golgi. These hydroxyproline residues (Hyp) can then be substituted with extensin-like O-glycans (substitution with arabinofuranoside by AraTs) or more complex arabinogalactan O-glycans, recently reviewed in Petersen et al. (2021). In contrast to animals, serine (S) and threonine (T) residues are not substituted with O-glycans in plants. GnTI, N-acetyl-glucosaminyltransferase I; GMII, Golgi-α-mannosidase II; GnTII, N-acetyl-glucosaminyltransferase II; XYLT, β1,2-xylosyltransferase; FUT11/12, Core α1,3-fucosyltransferase; GALT1, β1,3-galactosyltransferase; FUT13, α1,4-fucosyltransferase.
FIGURE 1 Glycosylation pathways in plants. A schematic overview of successive glycan modifying steps in the plant secretory pathway. Glycoproteins receive an N-glycan in the endoplasmic reticulum (ER) on an asparagine residue (N) within the consensus sequence (N-X-S/T), where X can be any amino acid except proline. After ER quality control, the correctly folded protein passes through the Golgi compartment. Within the Golgi immature high mannose-type N-glycans are modified in a tightly regulated process. First, Golgi α-mannosidase I (MNS1) trims down the N-glycan to a Man5 structure. In subsequent steps a diantennary N-glycan is synthesized, which in plants is substituted with core α1,3-fucose and β1,2-xylose. In some cases [as indicated by an asterisk (*)], this N-glycan is further extended with Lewis A motifs. Once secreted into the extracellular space (or apoplast) a terminal GlcNAc glycan structure can be trimmed down to a paucimannosidic glycan by the β-hexosaminidase HEXO3. Classical O-glycan synthesis in plants is initiated by the hydroxylation of proline residues by prolyl-4-hydroxylases (P4H) in the ER and/or Golgi. These hydroxyproline residues (Hyp) can then be substituted with extensin-like O-glycans (substitution with arabinofuranoside by AraTs) or more complex arabinogalactan O-glycans, recently reviewed in Petersen et al. (2021). In contrast to animals, serine (S) and threonine (T) residues are not substituted with O-glycans in plants. GnTI, N-acetyl-glucosaminyltransferase I; GMII, Golgi-α-mannosidase II; GnTII, N-acetyl-glucosaminyltransferase II; XYLT, β1,2-xylosyltransferase; FUT11/12, Core α1,3-fucosyltransferase; GALT1, β1,3-galactosyltransferase; FUT13, α1,4-fucosyltransferase.CC BY · PubMed Central
FIGURE 2 Diversity of helminth glycans. (A) A selection of N-glycan motifs found on different helminth glycoproteins. Besides immature mannosidic glycans, helminth N-glycans can be substituted with different core residues or are extended with different glycan motifs in their antenna. Some modifications are shared with animals, whereas other modifications are quite unusual. (B,C) A selection of O-glycan motifs found on different helminth glycoproteins, which are divided between typical core 1 (B) and core 2 (C) O-glycans. The linkage between different monosaccharides has been indicated where possible.
FIGURE 2 Diversity of helminth glycans. (A) A selection of N-glycan motifs found on different helminth glycoproteins. Besides immature mannosidic glycans, helminth N-glycans can be substituted with different core residues or are extended with different glycan motifs in their antenna. Some modifications are shared with animals, whereas other modifications are quite unusual. (B,C) A selection of O-glycan motifs found on different helminth glycoproteins, which are divided between typical core 1 (B) and core 2 (C) O-glycans. The linkage between different monosaccharides has been indicated where possible.CC BY · PubMed Central
FIGURE 3 Strategies to engineer helminth glycans. Schematic presentation of glycan engineering strategies for the synthesis of helminth N- and O-linked glycans in plants. In the green column plant wild-type glycan structures are depicted. To optimize the plant glycosylation pathway for “helminthisation” several genes need to be silenced by RNA interference or knocked out by genome editing techniques and these are indicated with Δ. From these different starting points glyco-engineering strategies have been illustrated to synthesize different mannosidic N-glycan structures, more complex structures with different antennary glycan motifs, and initiation of core 1 O-glycans. After choosing an appropriate plant line as starting point (either wild-type, RNAi line or genome edited), glyco-engineering commences by co-expression of different glycosyltransferases and/or glycosidases. The origin of each enzyme is given with two letter abbreviations for species names (Ce, Caenorhabditis elegans; Dm, Drosophila melanogaster; Dr, Danio rerio; Hs, Homo sapiens; Pa, Pseudomonas aeruginosa; Sm, Schistosoma mansoni; Tn, Tetraodon nigriviridus). No origin is given for plant endogenous enzymes. Enzymes: BGAL, β-galactosidase; HEXO, β-hexosaminidase; GnT, N-acetyl-glucosaminyltransferase; GalT, galactosyltransferase; GalNAcT, N-acetyl-galactosaminyl-transferase; FT, fucosyltransferase 11/12; FucT, fucosyltransferase; XT, xylosyltransferase. Other abbreviations or symbols: Asn, asparagine; Ser, serine; Thr, threonine; Pro, proline; Hyp, hydroxyproline; X, any amino acid; #, promoter strength for DrGalT determines the glycan composition, where control of expression with a dual 35S promoter results in hybrid glycans, but controlled expression with a weaker Gpa2 resistance gene promoter results in single-branched glycans. !: core a1,3-fucose is absent upon over-expression of DrGalT.
FIGURE 3 Strategies to engineer helminth glycans. Schematic presentation of glycan engineering strategies for the synthesis of helminth N- and O-linked glycans in plants. In the green column plant wild-type glycan structures are depicted. To optimize the plant glycosylation pathway for “helminthisation” several genes need to be silenced by RNA interference or knocked out by genome editing techniques and these are indicated with Δ. From these different starting points glyco-engineering strategies have been illustrated to synthesize different mannosidic N-glycan structures, more complex structures with different antennary glycan motifs, and initiation of core 1 O-glycans. After choosing an appropriate plant line as starting point (either wild-type, RNAi line or genome edited), glyco-engineering commences by co-expression of different glycosyltransferases and/or glycosidases. The origin of each enzyme is given with two letter abbreviations for species names (Ce, Caenorhabditis elegans; Dm, Drosophila melanogaster; Dr, Danio rerio; Hs, Homo sapiens; Pa, Pseudomonas aeruginosa; Sm, Schistosoma mansoni; Tn, Tetraodon nigriviridus). No origin is given for plant endogenous enzymes. Enzymes: BGAL, β-galactosidase; HEXO, β-hexosaminidase; GnT, N-acetyl-glucosaminyltransferase; GalT, galactosyltransferase; GalNAcT, N-acetyl-galactosaminyl-transferase; FT, fucosyltransferase 11/12; FucT, fucosyltransferase; XT, xylosyltransferase. Other abbreviations or symbols: Asn, asparagine; Ser, serine; Thr, threonine; Pro, proline; Hyp, hydroxyproline; X, any amino acid; #, promoter strength for DrGalT determines the glycan composition, where control of expression with a dual 35S promoter results in hybrid glycans, but controlled expression with a weaker Gpa2 resistance gene promoter results in single-branched glycans. !: core a1,3-fucose is absent upon over-expression of DrGalT.CC BY · PubMed Central

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  • Biopharmaceutical benchmarks 2018

    Walsh, G. (2018) · Nature Biotechnology · doi:10.1038/nbt.4305 · Cited by 978 · cited 1×

    “The majority of biopharmaceutical proteins are glycosylated (Walsh, 2018), a process where carbohydrate structures (glycans) are covalently attached to a protein backbone.”
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Metadata

Authors
van der Kaaij, A., van Noort, K., Nibbering, P., Wilbers, R. H. P., & Schots, A.
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2022-04-29
Volume
13
ISSN
1664-462X
DOI
10.3389/fpls.2022.882835
PMC
PMC9100689
Cited by
13
References
1
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

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