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Structural analysis of Escherichia coli O181 O-polysaccharide antigen
Ana Poceva Panovska
1
Supervisor: Göran Widmalm
2
1
Department of Organic chemistry, Faculty of Pharmacy, University Ss. Cyril and Methodius, 1000 Skopje, Macedonia
2
Department of Organic Chemistry, Arrhenius Laboratory, Stockholm University, S-106 91 Stockholm, Sweden
Lipopolysaccharides (LPS) are unique and abundant glycolipids found in the outer membrane of the Gram-
negative outer membrane. O-specific polysaccharide (O-antigen) of the LPS consists of a number of oligosaccharide
repeating units. There is an extensive variation in O-antigen structures, which is determined by the nature, order and
linkage of the different sugars within the polysaccharide. Structural studies of the O-specific polysaccharide of E.coli
have been of importance in understanding the role of this glycan in serological specificity and in pathogenesis.
The structure of the O-antigenic part of the lipopolysaccharide (LPS) obtained from the Escherichia coli
O181 has been partially determinated. 1H and 13C NMR spectroscopy techniques in combination with component
analysis were used to elucidate the O-antigen structure of O-deacylated LPS. 
Sugar analysis showed that PS contained four sugars: glucose, galactose, N-acetylglucosamine and N-acetyl-
galactosamine. There is significantly high amount of glucose present in the sample that may derive from the core
region of LPS or from the bacterial cell glycan. The absolute configuration analysis revealed that all sugars have 
D
-
configuration.
Elucidation of linkage position was revealed with methylation analysis. GC-MS spectra showed presence
of a 2-substituted hexose, 6-substituted hexose, 3 substituted 2-deoxy-2-N-methylacetamido hexose and 3,4-substi-
tuted 2-deoxy-2-N-methylacetamido hexose. One component from the methylation analysis could not be identified.
The 
1
H-NMR spectrum indicated presence of only 3 anomeric protons. Coupling constants for the anomer-
ic protons (J
H1,H2
3.8-4.0 Hz) showed that all sugars have anomeric protons in 
α–configuration. The anomeric pro-
ton at 5.52 ppm has an extra coupling, indicating the presence of phosphoric ester group. In the region 2.0-2.2 ppm
in
1
H-NMR spectrum, where methyl groups from acetyl substituents appear, four signals were observed with addi-
tional peaks at 1.28 and 1.30 ppm. The component analysis has not showed presence of 6-deoxy sugars, so we spec-
ulate that these signals may derive from alanine or other amino acid.
Since the phosphor ester groups were present we used selective hydrolysis with aqueous 48% HF at 4
°C.
The hydrolyzate was observed with MALDI-TOF MS using THAP (2,4,6-trihydroxyacetophenone) as a matrix, dur-
ing 24 hours intervals. After 24h peaks at m/z 1000 and 984 
[M
+
Na
] were observed indicating the molecular weight
of the repeating unit (hydrolysis product).
Further analyses are needed in order to determinate the complete structure of the biological repeting unit of
E.coli O181.
Macedonian pharmaceutical bulletin 53 (1,2) 16-17 (2007)
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Strukturna analiza na O-polisahariden antigen 
od Escherichia coli O181
Ana Poceva Panovska
1
Joran Vidmalm
2
1
Katedra za Organska hemija, Farmacevtski fakultet, 
Univerzitet Sv. Kiril i Metodij, 1000 Skopje, RMakedonija
2
Katedra za Organska hemija, Arenius laboratorii, Univerzitet vo Stokholm, S-106 91 Stokholm, [vedska
Lipopolisaharidite (LPS) se glikolipidi prisutni vo nadvore{nata membrana na Gram nega-
tivnite bakterii. O-specifi~niot polisaharid (O-antigenot) e sostaven del na LPS i se sostoi od nekolku
oligosaharidni povtoruva~ki edinici. Postoi {iroka varijabilnost na O-antigenskite strukturi koja e
odredena od prirodata, redot i na~inot na povrzuvawe na razli~nite monosaharidi prisutni vo polisa-
haridot. Strukturnite istra`uvawa na O-specifi~niot polisaharid na E.coli upatuvaat na ulogata na
ovoj glikan vo serolo{kata specifi~nost kako i vo patogenezata.
Delumno e opredelena strukturata na O-specifi~niot antigen izoliran od LPS-ot na Escherichia
coli O18. Koristeni se 1H i 13C NMR spektroskopski tehniki vo kombinacija so hemiska analiza na kompo-
nentite za rasvetluvawe na O-antigenskata struktura na O-deacetiliraniot LPS.
Analizata na {e}ernite komponenti poka`a prisustvo na 4 monosaharidi i toa glukoza, galak-
toza, N-acetilglukozamin i N-acetilgalaktozamin. Vo primerokot  e utvrdeno pogolemo prisustvo na
glukozata koja najverojatno poteknuva od sr`niot region na LPS-ot ili od glikanite prisutni vo bak-
teriskata kletka. Pri opredeluvawe na apsolutnata konfiguracija utvrdeno e prisustvo samo na {e}eri
so D-konfiguracija.
Za opredeluva mestoto na povrzuvawe na monosaharidnite edinici pome|u sebe se koristea metili-
ra~ki analizi. Spektrite dobieni so gaseno-masena spektroskopija  uka`uvaat na prisustvo na heksoza sup-
stituirana na pozicija 2 i pozicija 6, 3- supstituirana 2-deoksi-2-N-metilacetamido heksoza i 3,4-supsti-
tuirana 2-deoksi-2-N-metilacetamido heksoza. Edna od komponentite vo ovie analizi nemo`e{e da se
identifikuva.
1
H-NMR spektarot potvrdi prisustvo na samo 3 anomerni protoni odnosno tri {e}eri vo O-anti-
genot. Konstantite na spregnuvawe za anomernite protoni (J
H1,H2
3.8-4.0 Hz) uka`aa deka site {e}eri imaat
anomerni protoni vo a-konfiguracija. Anomerniot proton ~ij signal se javuva na 5.52 ppm ima dopolnitel-
no spregnuvawe {to upatuva na prisustvo na fosfoesterska grupa. Vo regionot od  2.0 - 2.2 ppm kade sig-
nali javuvaat metil grupite od acetil supstituentite vidlivi se ~etiri pikovi. Postojat i dopolnitelni
pikovi na 1.28 i 1.3 ppm. Bidejki pri analiza na komponentite ne se doka`a prisustvo na 6-deoksi {e}eri
ovie signali najverojatno poteknuvaa od alanin ili nekoja druga amino kiselina.
Poradi postoewe na fosfoesterski grupi koristena e i selektivna hidroliza so 48% voden  HF na
4 °S. Hidrolizatot e analiziran so MALDI-TOF masena sprektrometrija na sekoi  24 ~asa koristejki THAP
(2,4,6-trihydroxyacetophenone) kako matriks. Prvite pikovi  na hidrolizatot se jauvaat po 24 ~asa na m/z 1000
i 984 [M
+
Na] {to uka`uva na molekulskata masa na povtoruva~kata edinici (produktot na hidroliza).
Potrebni se dopolnitelni analizi do celosno rasvetluvawe na strukturata na biolo{kata povtoru-
va~ka edinica na O-antigenot na E. coli O181.
Macedonian pharmaceutical bulletin 53 (1,2) 16-17 (2007)
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Synthesis of monosaccharide units towards the synthesis 
of fucosylated N-linked hexasaccharide of a glycoprotein 
from Haemonchus contortus
Ana Poceva Panovska
1, 
Goran Widmalm
2
1
Department of Organic chemistry, Faculty of Pharmacy, University Ss. Cyril and Methodius, 1000 Skopje, Macedonia
2
Department of Organic Chemistry, Arrhenius Laboratory, Stockholm University, S-106 91 Stockholm, Sweden
Structural studies on the N-linked oligosaccharides of Haemonchus contortus, an economically important nem-
atode, have revealed a type core fucosylation not previously observed in any eukaryotic glycoprotein. The major N-
linked glycans identified, have up to three fucose residues attached to their cores. The latter substitution is unique in N-
glycans. This highly fucosylated core structure is expected to have unique properties and its synthetic analogues can be
used in immunological studies for vaccine development.
We report efficient and scalable synthetic protocols for preparation of monosaccharide precursors (thioglyco-
side and glycosyl azide) that can be used later, with some modification, for the synthesis of building blocks for the N-
glycan core structure present on the H. contortus glycoprotein. 
In the synthesis we optimized preparation of N–phthaloyl- and N –tetrachloropohthaloil (TCP)-D-glucosamine
tetraacetate, commonly used precursors in carbohydrate chemistry. The starting compound, glucosamine hydrochloride,
was converted into the protected intermediates phthalamate and tetrachlorophthalamate and further acetylated. After purifi-
cation the desired N-phthaloyl / TCP glucosamine tetraacetate was obtained in a high yield (80%) as predominant 
β-anomer
(J
H1,H2
9.028 Hz). The resulting products were further used for the preparation of glycosyl donors such glycosyl bromides,
1-thioglycosides and glycoside azides. To introduce an azide at C-1, the N-phthalimido peracetylated glycosamine was
treated with HBr/AcOH. Reaction resulted in formation of corresponding glycosyl bromide (yield 86%) as predominant-
ly 
β-anomer (J
H1,H2
9.4 Hz). Further, with the nucelophilic substitution of the bromide by sodium azide in dimethyl-
formamide (DMF), the reaction gave glycosyl azide as 
α-anomer (J
H1,H2
4.2 Hz). 
In order to obtain thioglycoside, often used as a glycosyl donor in glycosidation of aminosugars, acetylated
phtaloyl/tetrachlorophtaloil glucosamine reacted with thioethanol in the presence of the activator boron trifluoride diethyl
etherate BF
3
×Et
2
O (Lewis acids) and gave a good yield of the 1,2-trans product (
β-anomer, J
H1,H2
9.02 Hz).
Thioglycosides can be converted into other glycosyl donors. To convert the 
β-thioethyl glycoside into β-glycoside azide,
there are scalable published procedures performed in dichloromethane (DCM) using triflic anhydride NIS (N-iodosuc-
cinimide) as a promoter and sodium azide. These procedures did not count the possible formation azido-chloromethane
and diazidomethane as hazardous side products. In order avoid their formation we tested the azido displacement reac-
tion in solvents such as DMF and toluene. Latter reactions conditions did not result in expected products.
Macedonian pharmaceutical bulletin 53 (1,2) 18-19 (2007)
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Sinteza na monosaharidni edinici za sinteza na fukoziliran 
N
-povrzan heksasaharid prisuten kaj glikoprotein 
na Haemonchus contortus 
Ana Poceva Panovska
1
, Joran Vidmalm
2
1
Katedra za Organska hemija, Farmacevtski fakultet, 
Univerzitet Sv. Kiril i Metodij, 1000 Skopje, R. Makedonija
2
Katedra za Organska hemija, Arenius laboratorii, Univerzitet vo Stokholm, S-106 91 Stokholm, [vedska
Strukturnite istra`uvawa na N-povrzanite oligosaharidi od nematodata Haemonchus contortus
uka`uvaat na postoewe na karakteristi~na fukozilacija na nivnata sr` koja predhodno ne e utvrdena kaj
eukariotskite glikoproteini. Najgolemiot N -povrzan glikan koj e identifikuvan ima tri fukozni osta-
toci povrzani za negovata sr`. Ovaa visoko fukozilirana struktura se o~ekuva da ima edinstveni karak-
teristiki i nejziniot sintetski analog mo`e da se koristi vo imunolo{kite studii za razvoj na vakcini.
Vo ovoj trud vospostaveni se efikasni protokoli za sinteza na monosaharidni prekursori (tiog-
likozidi i glikozil azidi) koi ponatamu, so izvesni modifikacii, mo`e da se koristat kako gradbeni
edinici vo sinteza na N -glikanskata sr` prisutna kaj glikoprotein od H. contortus.
Optimizirana e postapkata za sinteza na dva naj~esto koristeni prekursori vo jaglehidratnata
hemija, N-ftaloil- i N-tetrahloroftaloil(TCP)- D-glukozamin tetraacetat. Kako pojdovno soedinenie
koristen e glukozamin hidrohlorid koj e  za{titen i preveden vo intermedierite ftalamat odnosno
tetrahloroftalamat i ponatamu e acetiliran. Po pre~istuvawe dobieniot N-ftaloil/TCP glukozamin
tetraacetat be{e dobien vo visok prinos (80%) i toa kako predominanten 
β-anomer (J
H1,H2
9.028 Hz).
Produktite dobieni vo ovoj ~ekor ponatamu se koristea za sinteza na glikozidni donori kako glikozil
bromidi, 1-tioglikozidi i glikozil azidi. Za voveduvawe na azido grupa na S-1, N-ftalimidoperacetili-
raniot glukozamin se tretira so HBr/AcOH. Kako produkt na ovaa reakcijata be{e dobien glikozil bromid
(prinos 86%) prete`no kako 
β-anomer (J
H1,H2
9.4 Hz). Ponatamu, preku supstitucija na bromidot so azid vo
dimetilformamid kako rastvoruva~ dobien e soodveten glikozil azid kako 
α-anomer (J
H1,H2
4.2 Hz).
Za sinteza na tioglikozidi, koi se koristat kako donori vo reakcii na glikozilirawe na amino-
{e}eri, acetiliraniot ftaloil/tetrahloroftaloil glukozamin  reagira{e so tioetanol vo prisustvo
na aktivator bor trifluorid dietileterat pri {to se dobi visok prinos na 1,2-supstituiran trans pro-
dukt (
β-anomer, J
H1,H2 
9.02 Hz). Tioglikozidite ponatamu mo`at da bidat konvertirani vo razli~ni
glikozidni donori. Za sinteza na glikozil azid od tioetil glikozid postojat pove}e objaveni protokoli
koi se izveduvaat vo dihlormetan pri {to se koristat i anhidrid na trifli~na kiselina, N-jodosukcin-
imid kako promotor i natrium azid. Vo ovie postapki ne e zemeno vo predvid mo`noto formirawe na eks-
plozivnite azido-hlorometan i diazidometan kako sporedni produkti. So cel da se izbegne nivnoto formi-
rawe reakcijata be{e izvedena vo rastvoruva~i kako toluen i dimetilformamid pri {to ne bea dobieni
o~ekuvanite produkti.
Macedonian pharmaceutical bulletin 53 (1,2) 18-19 (2007)
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Antiinflammatory and antidiabetic activity 
of Teucrium  polium extracts
Gjoshe Stefkov
1
, Anna Jager
2
, Per Molgaard
2
, Knud Josefsen
3
, Svetlana Kulevanova
1
1
Faculty of Pharmacy, Vodnjanska 17, Skopje, Macedonia
2
Faculty of Pharmaceutical Sciences, Jagtvej 162, 2200 Copenhagen, Denmark
3
Bartholin Institute, Panum, 2200 Copenhagen, Denmark
In vitro and in vivo examinations were done on the biological activity of dried extracts, lyophilized and spray-
dried basic water-ethanolic extract of Teucrium polium (Lamiaceae).
Antiinflammatory in vitro testing was done COX assay (reduction of the activity of cyclooxigenase 1 and
2-COX1 and COX2) and in vivo using the croton oil ear edema bioassay.
The agents that reduce the activity of COX1 or COX2 (enzymes which take place in production of prosta-
glandins), in most of the cases can exhibit an in vivo anti-inflammatory effect. The extract, added in a high concentra-
tion, has produce significant reduction of the activity of COX2, comparable with the effect of indometacin (anti-
inflammatory drug), but it did not show any effect on COX2.
Croton oil ear edema bioassay was done on mice and the difference in the weight of the patches (Ø=7mm)
from the treated (left) ear and the control (right) ear, was evaluated. The croton oil is an irritant which, applied super-
ficially on the skin produces an oedema. There is significant weight reduction of the patches from the treated with
extract ears compared with those untreated irritated ears, that suggests that the extract express superficial anti-inflam-
matory effect.
Evaluation of the anti-diabetic activity was done by in vitro examination of the insulinotropic effect of the
extract in cell lines and by in vivo examination of the same effect in mice. 
The measured concentration (ELISA method) of secreted insulin in INS-1E clonal cells, stimulated, with of
Teucrium polium extract or its fractions, has shown a significant increase of the quantity of secreted insulin (250 %-
350 %) cultured in the high glucose medium (20 mmol/L).
The in vivo anti-diabetic examinations were done by measuring plasma concentrations of glucose and insulin
in streptozotocin-diabetic mice. However, the plasma concentrations of glucose in mice, obtained after the admin-
istration of streptozotocin, were lower than the criteria that the mice can be assumed as being diabetic, and accord-
ingly the revealed concentrations of insulin and glucose, after the treatment with the extract, are insignificant.
The results from these examinations show the antiinflammatory and antidiabetic potential of the Teucrium
polium extracts.
Acknowledgment: All the research were done at the Faculty of Pharmaceutical Sciences and Bartholin
Institute, Panum, Copenhagen, Denmark as a part of the TEMPUS project for reconstruction of the pharmaceutical
education in Macedonia.
Macedonian pharmaceutical bulletin 53 (1,2) 20-21 (2007)
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Ispituvawe na antiinflamatorna i antidijabeti~na 
aktivnost na ekstrakti od Teucrium polium (Lamiaceae)
\o{e Stefkov
1
, 
Knul Jozefsen
3
, 
Ana Jager
2
, 
Pjer Molgard
2
, 
Svetlana Kulevanova
1
1
Farmacevtski fakultet, ul. Vodwanska 17, Skopje, Makedonija
2
Fakultet za farmacevtski nauki, ul. Jagtvej 162,2200 Kopenhagen, Danska
3
Bertolin institut, Panum, 2200 Kopenhagen, Danska
Vr{eni se in vitro i in vivo ispituvawa na biol{kata aktivnost na suvi ekstrakti (liofilizirani i
sprej-su{eni) dobieni od osnoven vodenoetanolen ekstrakt od Teucrium polium (Lamiaceae).
Procenka na antiinflamatornata aktivnost e izvr{ena preku in vitro testot za redukcija na aktivnos-
ta na ciklooksigenazata 1 i 2 (COX 1 i COX 2) i in vivo testot za povr{insko vosplaenie na uvo so krotono-
vo maslo.
Agensite {to in vitro ja reduciraat na aktivnosta na ciklooksigenazata 1 ili ciklooksigenazata 2
(enzim {to u~estvuva vo produkcija na prostaglandinite), mo`e da projavat in vivo antiinflamatoren efekt.
Ekstraktot, vo visoka koncentracija, postigna zna~ajna redukcija na aktivnosta na COX 2, sporedliva so
efektot na indometacinot (sporedben antiinflamatoren preparat), no ne poka`a efekt vrz COX 1.
In vivo antiinflamatoren test be{e izveden na gluv~iwa i be{e sledena razlikata vo masata na
tkivnite perforacii (
Ø = 7 mm) od levoto, tretirano uvo i od desnoto, kontrolno uvo. Krotonovoto maslo
e iritant koj nanesen povr{inski, na ko`ata, predizvikuva otok. Pomalata masa na tkivnite perforacii
od iritiranit u{i, tretirani so ekstraktot, od onaa od u{i na koi be{e nanesen samo iritant, uka`uva na
pozitiven povr{inski antiinflamatoren efekt.
Procenka na antidijabeti~nata aktivnost be{e izvr{ena preku ispituvawe na insulinotropniot
efekt na ekstraktot, in vitro na kleto~ni linii i in vivo na gluv~iwa.
Izvr{enoto merewe na koncentracijata na insulin so elisa metod poka`uva poka~uvawe na
koli~estvoto izla~en insulin kaj stimuliranite, INS-1E monoklonalni kletki, so ekstrakt od Teucrium poli-
um, vo odnos na kontrolnata grupa kletki, site postaveni vo uslovi na hiperglikemi~na sostojba.
In vivo antidijabeti~ni ispituvawa bea napraveni preku sledewe na plazma koncetraciite na insulin
kaj gluv~iwa, prethodno tretirani so streptozotocin za indukcija na dijabetes. O~ekuvanoto poka~uvawe
na plazma koncetraciite na glikoza kaj gluv~iwata, po administracija na streptozotocin, be{e ponisko
od kriteriumite da gluv~iwata bidat kartegorizrani kako dijabeti~ni i soodvetno na toa dobienite kon-
cetracii na insulin i glikoza, po tretmanot so ekstrakt, se insignifikantni.
Rezultatite od ovie istra`uvawa na uka`uvaat na potecijalot koj go poseduvaat ekstraktite od ovaa
rastenie so antiinflamatorni i antidijabeti~ni svojstva.
Blagodarnost: Site istra`uvawa bea napraveni za vreme na studiskiot prestoj na Fakultetot za
farmacevtski nauki i Panum institutot vo Kopenhagen, Danska, vo sklop na TEMPUS proektot za rekon-
strukcija na farmacevtskata edukacija vo Makedonija.
Macedonian pharmaceutical bulletin 53 (1,2) 20-21 (2007)
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Separation of metabolites of Ebselen in human and rat urine 
by LC-ICP-MS after solid phase extraction
Jasmina Tonic-Ribarska
1
, Suzana Trajkovic-Jolevska
1
, Kim Grimstrup Madsen
2
, Bente Gammelgaard
2
1
Faculty of Pharmacy, Ss Cyril and Methodius University, Vodnjanska 17, 1000 Skopje, Macedonia
2
Department of Pharmaceutics and Analytical Chemistry, Faculty of Pharmaceutical Sciences, 
University of Copenhagen, Universitetsparken 2, 2100 Copenhagen, Denmark
Selenium is an essential element that exerts it effect as the active center of selenoenzymes. In human plasma,
two major selenoproteins are present - Selnoprotein P and glutathione peroxidase. In these enzymes selenium is
incorporated as the selenoamino acid selenocysteine. Selenium also appears in other plasma proteins as selenome-
thionine, where this amino acid has been incorporated in competition with methionine as the organism is not able to
distinguish between these two amino acids. These proteins have no selenium-related function - albumin is an exam-
ple of such a protein. Besides being an essential micronutrient, selenium is known to have a cancer protective effect.
This effect is not related to the selenoproteins alone and current research has shown that monomethylated selenium
compounds may be the most efficacious in cancer prevention. However, the metabolism of selenium is not fully
understood. This project is part of the elucidation of how different selenium compounds are metabolized.
The purpose of this project was to investigate how Ebselen - an experimental drug with antioxidant and anti-
inflammatory properties - was metabolized in human urine compared to rat urine. A chromatographic method suit-
able for separation of the seleno-metabolites and compatible with ICP-MS was developed and different solid phase
extraction methods were compared for sample clean-up. Finally, it was tried to identify the metabolites by LC-MS.
When seleno-compounds like selenite and selenomethionine are ingested, the main urinary metabolite is a
seleno-sugar. When ingesting Ebselen, at least six different selenium-containing metabolites were observed in
human urine. The metabolic profiles of rat and human urine were different - fewer metabolites were observed in
rat urine. Unchanged Ebselen was not detected in both, human and rat urine. None of the metabolites co-eluted with
TMSe or the seleno-sugar that is normally the main metabolite in human and rat urine. Hence, Ebselen is metabo-
lized differently from selenite and selenomethionine.
Three different solid phase extraction cartridges were compared. Two of these did not change the metabol-
ic profile of human urine. Hence, samples could be cleaned by SPE without loosing metabolites.
When samples were analysed by LC-ESI-MS only one metabolite was detected (m/z 454) in human urine.
In rat urine, several metabolites were detected at m/z 454, 338, 404, 514 and 500. The difference is probably due
to the difference in total concentrations of the samples as the rat urine - the total selenium concentrations were 440
µg Se/L and 44600 µg Se/L respectively. Only the metabolites detected at m/z 454 and 338 have been reported
before. However, other metabolites have been suggested that were not detected in this study. This could be owing
to differences in mass spectrometric techniques as the formerly proposed structures werw suggested on basis of
electron ionization - much harder ionization method.
Macedonian pharmaceutical bulletin 53 (1,2) 22 (2007)
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