Institute of Biotechnology, P.O. Box 56, 00014 University of Helsinki, Finland
Received on August 8, 2000; revised on October 6, 2000; accepted on October 14, 2000.
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Abstract |
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Key words: chitin oligosaccharides/human 3-fucosyl-transferases/site-specific, peridistal
3-fucosylation
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Introduction |
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Results |
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Glycan 2' was reduced, permethylated, and subjected to ESI-MS. The [M+Na]+ ion (m/z 749.6) was selected for tandem mass spectrometry (MS/MS). The majority of the fragments produced could be assigned to the trisaccharide alditol GlcNAcß1-(Fuc1-)GlcNAcred (Figure 1A). The Y1a fragment (according to the nomenclature of Domon and Costello [1988]) at m/z 490.4 is produced by the loss of the nonreducing end GlcNAc. In addition, the Y1a/Y1b fragment at m/z 302.2 (as well as its dehydration product, m/z 284.2) will only arise from a doubly substituted GlcNAcred. However, small but clear ions (marked with an asterisk in Figure 1A) reveal also the presence of another isomer with fucose bonded to the nonreducing end GlcNAc. The Y1* ion (m/z 316.2) represents a singly substituted GlcNAcred, and the B2* ion at m/z 456.2 carries a disaccharide fragment representing the Fuc
1-GlcNAc unit from the the nonreducing end of the small side product. In conclusion, the MS/MS data established that Fuc-TV transferred mostly to the N-acetylglucosamine of the reducing end of N,N'-diacetylchitobiose.
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Also recombinant human Fuc-TVI converted Glycan 2 to Glycan 2'. This reaction, which was performed with 200 nmol of the acceptor and 400 nmol of the donor in 100 µl of the reaction mixture, afforded the purified product in an apparent yield of 180 nmol. The yield of the product was determined by its UV absorption at 214 nm, which was compared to the absorption of a GlcNAc reference. This method appears to overestimate the yield of the fucosylated products by about 20%. The 1D 1H NMR spectrum of the product was identical with that of the Fuc-TV-generated Glycan 2' (not shown). Human milk 3-fucosyltransferases, too, converted Glycan 2 to Glycan 2' that was isolated in pure form and identified by the 1D 1H NMR spectrum (not shown).
3-Fucosylation of N,N,N''-triacetylchitotriose (Glycan 3) by human Fuc-Ts
Incubation of Glycan 3 (1.0 µmol) with GDP-Fuc (1.0 µmol) and purified recombinant human Fuc-TV (25 mU) in 200 µl of the reaction buffer gave a mixture of oligosaccharides, from which 190 nmol of a purified tetrasaccharide product, Glycan 3', was isolated. The tetrasaccharide revealed in MALDI-TOF MS a major signal at m/z 796.5 that was assigned to [M+Na]+ of Fuc1GlcNAc3 (calc. m/z 796.3) (not shown).
Glycan 3' was reduced, permethylated, and subjected to electrospry ionization mass spectrometry (ESI-MS). The doubly charged [M+2Na]2+ ion (m/z 508.8) was selected for MS/MS. All fragments obtained could be assigned to the tetrasaccharide alditol GlcNAcß1-(Fuc1-)GlcNAcß1-GlcNAcred (Figure 1B). A loss of terminal, nonsubstituted GlcNAc unit is evident from the B1 ions at m/z 282.2 (sodiated) and m/z 260.0 (protonated). Loss of methanol from the m/z 260.0 ion accounts for the m/z 228.2 and m/z 196.2 ions. The Y1 ions at m/z 316.2 and m/z 338.2 (carrying one and two sodiums, respectively) indicate that the N-acetylglucosaminitol unit of the reduced Glycan 3' carried only one monosaccharide substituent. Furthermore, theY2a /B2 ion at m/z 442.4 can only arise by loss of a distal, unsubstituted GlcNAc accompanied by loss of the GlcNAcred unit. No fragments were observed, even in close inspection, which would represent a fucosylated reduced end (i.e., Fuc
1-GlcNAcred at m/z 490.4; cf. fragments of Glycan 2' in Figure 1A) or a fucosylated nonreducing end GlcNAc (at m/z 456.2). It is also noteworthy that fragmentation of the fucose unit produced mainly Z ions. This behavior is reportedly characteristic to 3-substitution (Viseux et al., 1997
), implying that the fucose was 1,3-linked to GlcNAc. The origin of the fairly intense fragment at m/z 455.2 is complex. Its nature was revealed by producing the B2, Y2a, and Z2b fragments with a high orifice voltage and by collecting MS/MS/MS data with these skimmer fragments (not shown). Only the Y and Z ions generated the m/z 455 ion, so it must contain the reduced end. We suggest that this is an 0,4X1 ion, arising by a cross-ring cleavage of the middle GlcNAc ring. Taken together, the MS/MS data established that Fuc-TV transferred exclusively to the middle GlcNAc of N,N,N''-triacetylchitotriose.
The 1D 1H-NMR spectrum of Glycan 3' (Table I) lacks the 4.144 p.p.m. H2-signal of the reducing end GlcNAc (i.e., unit C) of the -form of Glycan 2', confirming that the reducing end of Glycan 3' is different from that of Glycan 2'. By contrast, the H4 resonance of GlcNAc D in Glycan 3' is identical to that of Glycan 2', implying that the nonreducing ends in Glycans 2' and 3' are similar. Also the H1, H5, and H6 signals of fucose in Glycan 3' resemble their counterparts in Glycan 2'. Taken together, the NMR data confirm and extend the MS data, establishing that Fuc-TV-generated Glycan 3' represents GlcNAcß1-4(Fuc
1-3)GlcNAcß1-4GlcNAc. Human milk Fuc-Ts, too, converted Glycan 3 to Glycan 3', which was isolated in purified form and was identified by 1D 1H-NMR and MS/MS data (not shown).
3-Fucosylation of N,N',N'',N'''-tetraacetylchitotetraose (Glycan 4) by human Fuc-Ts
Glycan 4 (6 µmol) was incubated with GDP-Fuc (3 µmol) and partially purified Fuc-Ts of human milk (4.3 mU) in 1.2 ml of the reaction buffer for 2 days and with additional 4.3 mU of the enzyme for further 2 days. A mixture of oligosaccharides was obtained from which an isocratic high pH anion exchange run on a CarboPac PA-1 column, using 40 mM NaOH, gave 740 nmol of a pentasaccharide, Glycan 4'. It revealed in MALDI-TOF MS a major signal at m/z 999.7 that was assigned to [M+Na]+ of Fuc1GlcNAc4 (calc. m/z 999.4) (not shown).
Glycan 4' was reduced, permethylated, and subjected to ESI-MS. The doubly charged [M+2Na]2+ ion (m/z 631.6) was selected for MS/MS. The low-mass region of the MS/MS spectrum (Figure 1C) resembles that of Glycan 3', showing the same B1 fragments from the unsubstituted terminal GlcNAc unit (m/z 282.2, m/z 260.2), and Y1 ions from the GlcNAcred (m/z 316.2, m/z 338.2). In addition, theY2a /B2 ion (m/z 442.4), the B3 ion (m/z 946.8), and the Y3a ion (m/z 980.6) establish that the fucose unit is linked to either of the two midchain GlcNAcs. The Y2 ion at m/z 561.4 indicates that the GlcNAcß1-4GlcNAcred- fragment originally carried only one saccharide substituent, implying that the fucose must reside at the penultimate GlcNAc residue C, close to the nonreducing end. This notion is directly confirmed by the B2 ion at m/z 701.6, carrying the methylated fragment GlcNAcß1-(Fuc1-)GlcNAc derived from the nonreducing terminus of Glycan 4'. As above, fragmentation of the fucose unit produced Z ions, implying the presence of a Fuc
1,3-linkage. The MS/MS data did not reveal any specific fragments for other pentasaccharide isomers. We conclude that Glycan 4 was fucosylated solely to the penultimate GlcNAc residue next to the nonreducing end.
1D 1H-NMR spectrum of purified Glycan 4' (Table I) was analogous to that of Glycan 3'. The proton signals of the fucose and the GlcNAc D (Table II) were assigned as described by Maaheimo et al. (1997). The data reveal a great similarity in the spin systems of the fucose and the GlcNAc D in Glycans 2' and 4'. In addition, the ROESY spectrum of Glycan 4' (not shown) revealed cross peaks between fucose H5 and GlcNAc D H2 as well as between fucose H6 and GlcNAc D H2 (compare Table III), suggesting that the fucose and the GlcNAc D are stacked also in Glycan 4'. Taken together, the NMR data confirm and extend the MS/MS results, establishing that Glycan 4' represented GlcNAcß1-4(Fuc
1-3)GlcNAcß1-4GlcNAcß1-4GlcNAc.
Even Fuc-TV converted Glycan 4 to Glycan 4', which was isolated in purified form in a yield of 22% and was identified by its 1D 1H-NMR spectrum (not shown).
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Discussion |
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Eq. 1. GlcNAcß1-4GlcNAcß1-OR + GDP-Fuc
GlcNAcß1-4(Fuc1-3)GlcNAcß1-OR + GDP
The fucose unit was transferred selectively to the N-acetylglucosamine unit adjacent to the nonreducing end in all three chitin oligosaccharide acceptors. No other isomers were observed in Glycans 3' and 4', the fucosylated products from N,N'N''-triacetylchitotriose and N,N',N'',N'''-tetraacetylchitotetraose, respectively. However, Glycan 2', the fucosylated N,N'-diacetylchitobiose, GlcNAcß1-4(Fuc1-3)GlcNAc, was contaminated by a small amount of an isomeric side product where the fucose was linked at the nonreducing end GlcNAc of the acceptor.
Even a soluble form of recombinant human Fuc-TVI, and partially purified human milk Fuc-Ts catalyzed the reactions of Equation 1. It is not known at present whether these Fuc-Ts generate also the distally fucosylated side product when working with N,N'-diacetylchitobiose.
The products of Fuc-T reactions were characterized by MALDI-TOF MS, ESI-MS/MS, and 1D as well as 2D-NMR experiments. The NMR data confirmed that the Fuc-Ts, working with the chitin oligosaccharides, generated Fuc1-3GlcNAc linkages rather than Fuc
1-6GlcNAc bonds. The novel reactions of Equation 1 are analogous to the reactions of neutral i-type polylactosamine chains catalyzed by several human Fuc-Ts. Even these acceptors are
3-fucosylated at the peridistal N-acetylglucosamine unit by several human Fuc-Ts (Niemelä et al., 1998
; Nishihara et al., 1999
). However, many human Fuc-Ts transfer efficiently even to inner N-acetyllactosamine units of i-type polylactosamine chains, e.g., to the middle GlcNAc of the hexasaccharide Galß1-4GlcNAcß1-3Gal-ß1-4GlcNAcß1-3Galß1-4GlcNAc (de Vries et al., 1995
; Niemelä et al., 1998
; Nishihara et al., 1999
). Remarkably, the present experiments with Glycan 4 did not lead to transfer at sites other than the peridistal GlcNAc, implying that a difference exists in the acceptor activities of the nondistal parts of chitin saccharides and i-type polylactosamines.
There are some predecessors of the present findings. N,N'-diacetylchitobiose was fucosylated by a human lymphocyte enzyme (Hoflack et al., 1978), that was probably an
3-fucosyltransferase; the known
6-fucosyltransferases do not react with N,N'-diacetylchitobiose (Voynow et al., 1991
). Fucosylation of some chito-type saccharides by human Fuc-TVI (Nimtz et al., 1998
) and fucosylation of N,N'-diacetylchitobiose-6-sulfate (Tran et al., 1998
) have also been reported.
The site-specific and efficient transfer of 3-linked fucose to chitin oligosaccharides of the present experiments generated products that resemble a Nod factor of Mesorhizobium loti (Olsthoorn et al., 1998
) but are distinct from the
6-fucosylated nodulation signals synthesized from chitin oligosaccharides by the NodZ enzyme (Quinto et al., 1997
). Indeed, in the history of life, chitin oligosaccharides may have been the first acceptors for
3-fucosyltransferases, which are highly conserved from bacteria to humans (Oriol et al., 1999
; Leiter et al., 1999
). Consequently, the present-day glycoconjugates with N-acetyllactosamine units may be relatively late "clients" of these enzymes. Additional acceptors for these enzymes may be available in saccharide sequences like cello-oligosaccharides, laminaribiose, Manß1-4GlcNAc, and GlcUAß1-3GlcNAc.
The present ROESY data (summarized in Table III) suggest that the fucose and the distal GlcNAc residue in the 3-fucosylated chitin saccharides are stacked in a way reminiscent of the stacking of fucose and galactose in the Lewis x determinant (Wormald et al., 1991
; Miller et al., 1992
). Analogous interactions have been reported also in the GalNAcß1-4(Fuc
1-3)GlcNAc epitope (Bergwerff et al., 1993
), in the
3-fucosylated core of plant N-glycans (Bouwstra et al., 1990
), and in the Nod-factor lipo-oligosaccharide from M. loti (Olsthoorn et al., 1998
). All these examples of uniquely rigid trisaccharide determinants are probably recognized by several proteins and perhaps also by other saccharides; the details are best understood for the Lewis x binding. For instance, the rigidity of the GlcNAcß1-4(Fuc
1-3)GlcNAc determinant in the core of N-glycans in plants may contribute importantly to the allergenicity characteristic for many plant glycoproteins (Garcia-Casado et al., 1996
; van Ree et al., 2000
). On the other hand, the
3-fucosylation of chitin oligosaccharides is likely to restrict the action of chitinases, ß4GlcNAc transferases, acyl transferases, and lectins recognizing chitin-type chains; analogous effects of
3-fucosylation on polylactosamine binding are well known (reviewed in Renkonen, 2000
).
The in vitro Fuc-T reactions with chitin oligosaccharides and their derivatives may prove useful for synthesis of man-made plant growth regulators (Röhrig et al., 1995; Staehelin et al., 1994
) and elicitors of defense functions (Yamaguchi et al., 2000
). Developmentally important derivatives of N-acetyl-chito-oligosaccharides are believed to occur even in vertebrates, but their exact structures are not known (Semino et al., 1996
), and no functional relations between these saccharides and the
3-fucosyltransferases are known at present.
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Materials and methods |
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Fucosyltransferase reactions
Fuc-TV reactions were carried out under conditions similar to those described by Palcic et al. (1989); the nominal enzyme concentrations were initially 12.5 mU/100 µl, and the reaction mixtures were incubated for 5 days at room temperature. In Fuc-TVI reactions, the nominal enzyme concentration was initially 10 mU/100 µl, and the reaction mixtures were incubated for 3 days at 37°C. For human milk Fuc-T reactions, Glycan 2 was incubated with the enzyme at 10 mM and Glycans 3 and 4 at 5 mM; the initial enzyme concentration was typically 360 µU/100 µl and fresh enzyme (360 µU/100 µl) was added after 2 days; the incubations were performed at 37°C for a total of 4 days.
Chromatographic methods
Chromatographic experiments were performed as described by Maaheimo et al. (1995) and Natunen et al. (1997)
.
Mass spectrometry
MALDI-TOF MS was performed in the positive ion delayed extraction mode with a BIFLEXTM mass spectrometer (Bruker-Franzen Analytik, Bremen, Germany) using 2,5-dihydroxybenzoic acid as the matrix. ESI-MS of reduced and permethylated (Ciucanu and Kerek, 1984) glycans were collected using an API365 triple quadrupole mass spectrometer (Perkin-Elmer Instruments, Thornhill, Ontario). The samples were dissolved in 50% aqueous methanol containing 0.5 mM sodium hydroxide and injected into the mass spectrometer with a nanoelectrospray ion source (Protana A/S, Odense, Denmark) at a flow rate of about 30 nl/min. MS/MS spectra were acquired by colliding the selected precursor ions to nitrogen collision gas with acceleration voltages of 35 V (doubly charged precursors) or 55 V (singly charged precursors).
NMR spetroscopy
The NMR experiments were performed on a Varian Unity 500 spectrometer at 23°C in Shigemi tubes (Shigemi Co., Tokyo) essentially as described in Maaheimo et al. (1997). The assignments are based on the structural reporter group resonances of Table I and DQFCOSY, TOCSY, 1D selective TOCSY, HSQC, 2D HMQC-TOCSY and DEPT 135 experiments.
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Acknowledgments |
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Abbreviations |
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Footnotes |
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2 To whom correspondence should be addressed
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References |
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