Further insights on structural modifications of muramyl dipeptides to study the human NOD2 stimulating activity
Wei-Chieh Cheng, Ting-Yun You, Zhen-Zhuo Teo, Ashik A. Sayyad, Jitendra Maharana, Chih-Wei Guo, Pi-Hui Liang, Chung-Shun Lin, and Fan-Chun Meng
[a] Prof. Dr. W.-C. Cheng, T.-Y. You, Z.-Z. Teo, Dr. A.-A. Sayyad, C.-W. Guo, C.-S. Lin, F.-C. Meng Genomics Research CenterAcademia SinicaNo. 128, Academia Road Sec. 2, Nangang District, Taipei, 115 (Taiwan)
[b] Z.-Z. Teo, Prof. Dr. P.-H. Liang School of PharmacyNational Taiwan UniversitNo. 17, Xuzhou Road, Taipei, 106 (Taiwan)
[c] Prof. Dr. W.-C. Cheng Department of Chemistry National Cheng-Kung UniversityNo.1, University Road, Tainan, 701 (Taiwan)
[d] Prof. Dr. W.-C. Cheng Department of Applied Chemistry National Chiayi UniversityNo. 300, Syuefu Road, Chiayi, 600 (Taiwan)
[e] Prof. Dr. W.-C. ChengDepartment of Medicinal and Applied Chemistry Kaohsiung Medical UniversityNo.100, Shin-Chuan 1st Road, Kaohsiung, 807 (Taiwan)
[f] Jitendra MaharanaInstitute of Biological Chemistry Academia SinicaNo. 128, Academia Road Sec. 2, Nangang District, Taipei, 115 (Taiwan)
[g] Jitendra MaharanaTaiwan International Graduate Program (TIGP), Chemical biology and molecular Biophysics (CBMB) Academia SinicaNo. 128, Academia Road Sec. 2, Nangang District, Taipei, 115 (Taiwan)
[h] Jitendra MaharanaInstitute of Bioinformatics and Structural Biology National Tsing Hua UniversityNo. 101, Sec. 2, Guangfu Rd., Hsinchu, 300 (Taiwan)
Abstract:
A series of muramyl dipeptide (MDP) analogues with structural modifications at the C4 position of MurNAc and on the D- iso-glutamine (isoGln) residue of the peptide part were synthesized. The C4-diversification of MurNAc was conveniently achieved by using CuAAc click strategy to conjugate an azido muramyl dipeptide precursor with structurally diverse alkynes. D-Glutamic acid (Glu),replaced with isoGln, was applied for the structural diversity throughesterification or amidation of the carboxylic acid. In total, 26 MDP analogues were synthesized and bio-evaluated for the study of human NOD2 stimulation activity in the innate immune response. Interestingly, MDP derivatives with an ester moiety are found to be more potent than reference compound MDP itself or MDP analogues containing an amide moiety. Among the varied lengths of the alkyl chain in ester derivatives, the MDP analogue bearing the D- glutamate dodecyl (C12) ester moiety showed the best NOD2 stimulation potency.
Introduction
Peptidoglycans (PGNs) are the major components of bacterial cell walls. They comprise of a repeating disaccharide unit commonly known as N-acetyl glucosamine-(1→4)-N-acetyl- muramic acid, which is cross-linked by short peptide chains (in many Gram-positive bacteria the third amino acid is L-Lys; in most Gram-negative bacteria it is meso-DAP) to form the rigid structure of the cell wall.1,2 The PGNs as well as these biomolecules are potential pathogen-associated molecular patterns (PAMPs), which can be recognized by pattern recognition receptors (PRRs) to induce immune response.3,4 During bacterial infection, PGNs and their fragments are recognized by PRRs, located on either the membrane surface, like TLR2, NLRP3 and other peptidoglycan recognition proteins, or inside the cytoplasm, like Nucleotide-binding oligomerization domain-containing protein 2 (NOD2) and NOD1.5–8 The NOD2 gene is the first gene to be identified to associate with Crohn’s disease (CD) susceptibility,9 and recent studies revealed that functional loss of NOD2 due to mutations correlates with Crohn’s disease, a chronic inflammatory gastrointestinal disease.10,11
Results and Discussion
GMDP, which structurally contains the glycosyl moiety (GlcNAc) at the C4 position of MurNAc, prompted us to further investigate the effect of C4 substitution of MDP on NOD2 stimulation activity. Previous works demonstrated the modifications or the removal of the methyl group on the lactate of MurNAc and (or) on L-Ala of the peptide part in MDP could dramatically impair the activity by us and others (Figure 2).27,28
Scheme 1. Synthetic route for the preparation of azide 8. Reagents and conditions: (a) i. NaOMe, Ac2O, MeOH, 2 h, rt; ii. BnOH, HCl, 80 °C, 75% over2 steps; (b) i. PhCHO, ZnCl2, rt; ii. NaH, 2-(S)-chloropropionic acid, 1,4- dioxane, 70 °C, 73% over two steps; (c) i. H-Ala-OTMSE, HBTU, Et3N, CH2Cl2/THF, rt; ii. p-TSA, MeOH, 60 °C, 0.5 h; ii. BzCl, pyridine, CH2Cl2,−78 °C to rt, 60% over 2 steps; (d) i. Tf2O, pyridine, 0 °C, 1 h; ii. NaN3, DMF, 60 °C, 24 h, 73% over two steps; (e) i. TBAF, THF, 30 min, rt; ii. D-isoGln(OBn), HBTU, HOBT, DIPEA, CH2Cl2, rt, 4 h, 60% over two steps; (f) 2 N LiOH(aq), THF/MeOH=1:1, 50%.
As shown in scheme 1, benzyl N-acetyl-D-galactosamine 3, was prepared from D-galactosamine (D-GalN) following the literature procedure.29 After benzylidination of 3, followed by O- alkylation at the C3-hydroxy position with 2-(S)-chloro-propionic acid under basic condition (NaH, 1,4-dioxane, 70 oC), acid 4 was obtained in 73% yield over two steps. Subsquently, 4 wascoupled with H-Ala-OTMSE in the presence of HBTU, followed by benzylidene acetal deprotection and selective O- benzoxylation at the C6-hydroxy group gave 5 in 60% yield over two steps. The Lattrell-Dax protocol30 was utilized to convertalcohol 5 into azide 6 through the O-triflation in 73% yield over two steps. After TMSE deprotection of 6 with TBAF, the intermediate was coupled with γ-benzyl-D-isoglutamine in the presence of HBTU and HOBT to give 7 in 60% yield over two steps. Compound 7 was hydrolyzed under basic condition to afford azide 8 in moderate yield.
To achieve the desired C4-substituent diversity in MDP analogues initially conjugation with various alkyl and aryl isocyanates was planned. Towards this endeavor, the required amine precursor 9 was obtained from azide 8 via Staudinger reaction in 61% yield. Unfortunately, our attempt to conjugate amine 9 with an isocyanate such as 1-isocyanato-3- methoxybenzene, did not work well; presumably due to the C4 steric hindrance hampering the reactivity of amine 9. To overcome this difficulty in C4 diversification, we adopted the copper (I)-catalyzed azide alkyne cycloaddition (CuAAC) strategy. Accordingly, when azide 8 was conjugated with a terminal alkyne, 2-(4-methoxyphenyl)-N-(prop-2-yn-1-yl)aceta- mide, smoothly generated required triazole 10 in 63% yield (Scheme 2).
Scheme 3. Synthetic route of C4 diversified MDP 11 to 14 via click reaction. Reagents and conditions: (a) alkynes, CuSO4∙5H2O, sodium ascorbate, MeCN/H2O=1:1, 80 ºC, 24 h; (b) H2 (80 psi), Pd(OH)2/C, MeOH, cat. AcOH, rt, 24 h.
The MDP analog 17 with the O-benzyl moiety at C-1 position was prepared via EDCI mediated amide coupling reaction in between acid 1531,32 and amine 16 and further debenzylation of 17 afforded MDP (1) in 55% yield over two steps as depicted in scheme 4.
With this successful model reaction in hand, azide 8 was further subjected for parallel conjugation reactions with different readily prepared alkynes through the CuAAC protocol, followed by global deprotection to achieve the desired C4-substituted (alkyl, aryl, with amide group, and with secondary amine group) MDP analogues 11-14 in moderate to good yields as presented in scheme 3might play an important role for the NOD2 stimulation activity. Indeed, the activity potency of 8, 9, and 10 were not attractive and azide 8 exhibited a weak response only at 1000 nM concentration.
After analyzing these primary results, next we moved our attention to the structural modification of the dipeptide part on MDP as planned. Based on our structural design and the similar synthetic route in scheme 4, six MDP analogues (18-23, Figure 4) were prepared. Notably, 15 was used as a common precursor, and protected dipeptides containing L-glutamic acid, D-glutamic acid or D-aspartic acid as building blocks were utilized.
The biological results of MDP analogues 18-23 were shown in figure 5 and MDP (1) was applied as our reference compound. A brief summary was as follows: (1) When the D-chirality of iso- glutamine was changed to the L-form, the activity was found to be reduced (MDP (1) vs. 22), and this result is consistent with early reported in the literature.27 (2) The NOD2 stimulation activity dramatically lost for the MDP analogues possessing the shorter alkane spacer in the second amino acid from iso- glutamine to iso-asparagine (MDP (1) vs. 23). (3) Analogue 21 bearing the iso-glutamine 5-ethyl ester moiety exhibited the less activity potency than MDP (1) with the free carboxylic acid of iso- glutamine. (4) The activity potency of MDP analogue 20 bearing glutamic acid manifested the similar results compared to MDP, which implied that the carboxylic acid might be a surrogate moiety of unsubstituted amide. (5) Gratifyingly, analogue 19 bearing the diethyl glutamate was found to be slightly more potent than MDP (1) at low concentration (10 nM and 100 nM), whereas analogue 18 (10 nM) with the only monoethyl ester moiety displayed a stronger activity than both MDP (1) and analogue 19 (Figure 5)
These exciting results (Figure 5), especially the structures ofcontaining a glutamate ester moiety with a varied carbon alkyl chain length (C8-32, C12-33, C16-34, and C20-35). Our biological results are displayed in figure 9. Impressively, at the lower concentration (10 nM), MDP (1) and its accessible analogue, Murabutide (MB, MurNAc-L-Ala-D-GlnOBu)33 were found to be inactive but our newly synthesized MDP analogues with an alkyl ester moiety presented increased activity potency. All the MDP analogues (18, 24, 32-35) were more active than MDP (1) and MB. In addition, we observed that MDP analogues bearing a longer alkyl chain lead to the better activity and the compound possessing the C12 alkyl chain reached to the best possible potency. The similar trend of the NOD2 stimulation activity was also observed at 100 nM concentration. Notably, the activity potency of 34 and 35 did not demonstrated a clear trend; presumably due to the hydrophobic property of the longer alkyl chain (C16 and C20) of 34 and 35 (1000 nM) might be inducing some non-specific interactions or even leading to aggregationactive hits (18 and 19), inspired us for further study the structural modifications of MDPs. Following the similar synthetic approaches we described above, eight MDP analogues including four O-substituted derivatives and four N- monosubstituted derivatives (analogues 24-31, Figure 6) were prepared. The bio-evaluation results are shown in figure 7. Compared to 18, MDP analogue 24 with a longer alkyl chain in the O-substituted glutamate ester demonstrated a better activity.
In contrast, MDP analogue 25 with the chlorinated ethyl ester did not significantly increase the activity. MDP analogue 26 with a cyclohexane moiety or 27 with a phenethyl group presented the similar activity potency with analogue 19 even at higher concentrations (100 nM and 1000 nM). However, at the concentration of 10 nM, analogues 26 and 27 displayed slightly better activity potency than 18. Notably, analogues 25, 26, and 27 exhibited stronger potency than reference compound MDP (1), even at a lower concentration (10 nM). Surprisingly, MDP analogues which structurally contain a N-mono-substituted amide moiety including a varied alkyl chain (28 and 29), a cyclohexyl moiety (30), and a fluorine-containing alkane (31) were found to be inactive and these compounds illustrated some weak activities only at a higher concentration (1000 nM). Our observations indicated this one atom difference (O vs. N) in structurally similar MDP analogue pairs such as 24 vs. 28 or 26 vs. 30 dramatically affected the NOD2 stimulation activity for unknown reasons. Further studies such as their stability or permeability test remained to be investigated in the future.
Next, we took advantage of recent reports of the crystal structure of NOD2 to study the putative binding mode of 33 through our computational modeling.34 The concave surface of NOD2LRR (comprising of R823, F851, R877, G879, G905, W907, W931, S933, V935, E959, K989, S991 and C961 residues) isrequired for MDP recognition.23,35–37 As displayed in Figure 10, we observed both 1 and 33 are interacting in a similar fashion. In a similar line with previous predictions,23,36 we observed the MurNAc moiety of 1/33 found in a hydrophobic pocket (F851, W907 and W931 residues). The L-Ala-D-iGln part was found interacting with a positively charged pocket that involves R823, R877 and K989 residues. Further, in case of 33, the C12 tail part was found to be placed in a hydrophobic pocket (F903, Y821, K847 A875, and W911 residues).
Figure 10. Predicted binding mode of (A) MDP (1) and (B) 33 on the concave surface of NOD2LRR. Left panel indicates the 3D model interaction model, where the protein is visualized in gray cartoon, key interacting residues in ball- stick model (cyan) and the ligands are displayed in colored sticks models (1; yellow and 33; lime). Right panel indicates the interaction of 1/33 with NOD2LRR in 2D, where the key H-bond forming residues, 1 and 33 are displayed in line-art model, and the residues with hydrophobic interactions are showed in half-circles. The polar contacts or H-bonds are indicated in orange dashed lines and residues in parenthesis are of human NOD2.
Conclusions
We have successfully performed extensive structural modifications of MDP at the C4 position of MurNAc and on iso- glutamine (isoGln) residue of the peptide part. A convenient method for the diversification at the C4 position of MurNAc was developed through a CuAAC click strategy to conjugate an azido muramyl dipeptide precursor with a wide range of structurally diverse alkynes. Although the substituted triazole moiety at the C4 position of MDP analogues did not exhibit promising results for NOD2 stimulation activity, our strategy could be useful for structural diversity of MurNAc or other monosaccharide analogues towards other research purposes or applications.
Besides these studies, we also performed the systematic modifications of the iso-glutamine (isoGln) moiety in MDP analogues, applied for the human NOD2 stimulation activity in the innate immune response. Delightfully, MDP derivatives with a substituted ester moiety are observed to be more potent than the reference compounds (MDP and MB) and the other MDP analogues containing an amide moiety. Interestingly, the general trend manifested MDP analogues bearing a longer alkyl chain in the D-glutamate ester moiety led to the better NOD2 stimulation activity. Among our synthetic MDP analogues, the most potent NOD2 activator was the MDP analogue bearing the D-glutamate dodecyl (C12) ester moiety. This new finding and new NOD2 activators would allow us to use them as chemical probes or ligands for further studies in the innate immune system, cytokine expression pattern, or autophagy research in the future. These results will be reported in due course.
Experimental Section
General Information
All solvents and reagents were obtained commercially and used without further purification. All reactions were monitored by analytical thin-layer chromatography (TLC) plates with silica gel 60 F254. TLC plates were visualized by the exposure of ultraviolet light at 254 nm or by the immersion of staining solution (p-anisaldehyde, acidic ninhydrin, phosphomolybdic acid, or potassium permanganate) followed by heating. After the completion of all reactions, solvents were removed by rotary evaporation. The crude products were purified by column chromatography (cc) with 40–63 μm silica gel. NMR spectra were recorded by the Bruker AVANCE 600 spectrometer at ambient temperature. 1H NMR spectra were referenced with deuterated solvents such as chloroform-d (δ=7.26), methanol-d4 (δ=3.31), and deuterium oxide (δ=4.79). 13C NMR were referenced with chloroform-d (δ=77.23 ppm of central line) and methanol-d4 (δ=49.15 ppm of central line). High- resolution mass spectra were obtained by the Bruker Daltonics BioTOF III spectrometer (ESI-MS). HEK-Blue hNOD2 cells were incubated with different concentrations of MDP analogues for 16 h. SEAP (secreted alkaline phosphatase) were quantified as described in supporting information. Data are presented as mean ± standard deviation (SD) (n = 3). Synthetic procedures (3→7 and 15→17) and preparation of dipeptides (S1-S17) are shown in the supporting information.
Compound 8. LiOH(aq) (2.0 N, 0.47 mL, 0.94 mmol) was added to thesolution of 7 (0.15 g, 0.19 mmol) in MeOH/THF (10 mL, v/v = 1:1). After 1 h, the mixture was neutralized by Dowex 50WX8 resin, and then the filtrate was concentrated. The crude product was purified by cc (n- PrOH/H2O = 40:1 to 20:1, silica gel) to give 8 (72 mg, 0.12 mmol, 63%) as a white solid; 1H NMR (600 MHz, D2O) δ 7.35-7.28 (m, 5H), 4.78 (d, J
= 3.5 Hz, 1H), 4.61 (d, J = 12.0 Hz, 1H), 4.43 (d, J = 12.0 Hz, 1H), 4.22-
4.10 (m, 3H), 4.02-3.98 (m, 1H), 3.79-3.75 (m, 1H), 3.72-3.71 (m, 2H),
3.63-3.55 (m, 2H), 2.22-2.15 (m, 2H), 2.09-2.02 (m, 1H), 1.86-1.81 (m,
4H), 1.39-1.32 (m, 6H); 13C NMR (150 MHz, D2O) δ178.0, 175.8, 175.3,
174.4, 173.7, 136.8, 128.7, 128.6, 96.0, 95.8, 78.7, 78.0, 70.5, 69.7, 61.1,
60.6, 53.4, 52.7, 49.5, 31.2, 21.83, 21.80, 18.3, 18.2, 16.7, 16.6; HRMS (ESI-TOF) m/z calcd for C26H37N7O10 + H+: 608.2675 [M+H]+; found: 608.2676.
Compound 9. Triphenylphosphine (17 mg, 0.066 mmol) was added to the solution of 8 (20 mg, 0.033 mmol) in THF/H2O (1 mL, v/v = 3:1), and the reaction was refluxed at 65 °C. After 24 h, the reaction mixture was concentrated. The residue was purified by cc (n-PrOH/H2O = 20:1 to 7:1, silica gel) to afford 9 (15 mg, 0.026 mmol, 78%) as a white solid; 1H NMR (600 MHz, D2O) δ 7.37-7.32 (m, 5H), 4.80 (s, 1H), 4.65 (d, J = 11.9 Hz,
1H), 4.49 (d, J = 11.9 Hz, 1H), 4.14-4.08 (m, 3H), 4.06-4.04 (m, 2H),
3.91-3.89 (m, 2H), 3.73 (d, J = 3.7 Hz, 2H), 3.35-2.98 (m, 1H), 2.21-2.13
(m, 2H), 2.03-1.99 (m, 1H), 1.86-1.80 (m, 1H), 1.77 (s, 3H), 1.38 (s, 3H), 1.36 (s, 3H); 13C NMR (150 MHz, D2O) δ 178.5, 178.3, 177.7, 175.3,
173.8, 136.7, 128.7, 128.6, 128.4, 96.0, 77.6, 77.4, 69.8, 60.5, 54.5, 54.3,
53.3, 53.2, 51.5, 49.6, 49.5, 31.4, 31.3, 27.8, 27.7, 21.8, 18.8, 18.7, 16.6,
16.3; HRMS (ESI-TOF) m/z calcd for C26H39N5O10 + H+: 582.2770 [M+H]+;
found: 582.2772.
Compound 10. N,N-Diisopropylethylamine (0.42 mL, 2.4 mmol) was added to the mixture of propargylamine (0.13 mL, 2.0 mmol), 4- methoxyphenylacetic acid (2.0 mmol), and EDCI (0.46 g, 2.4 mmol) in dry CH2Cl2 (5.0 mL). The mixture was stirred at rt. After 12 h, the mixture was quenched and washed with 1.0 N HCl(aq), and the organic layer was collected, dried over magnesium sulfate, and concentrated. The residue was directly applied for next step without further purification. The mixture of the residue (20 mg, 0.099 mmol), CuSO4(aq) (1.0 M, 3.3 μL, 0.0033 mmol) and sodium ascorbate(aq) (1.0 M, 9.9 μL, 0.0099 mmol) was added to the solution of 8 (20 mg, 0.033 mmol) in MeCN/H2O (0.33 mL, v/v = 1:1). The reaction mixture was stirred at 80 °C. After 24 h, the reaction mixture was concentrated and purified by cc (n-PrOH/H2O = 20:1 to 7:1, silica gel) to afford 10 (17 mg, 0.021 mmol, 63%) as a white solid; 1H NMR (600 MHz, CDCl3) δ 7.86 (d, 1H, J = 6.6 Hz), 7.47-7.41 (m, 5H),
7.19 (d, 2H, J = 7.8 Hz), 6.92 (d, J = 8.4 Hz, 2H), 5.0 (s, 1H), 4.81 (s, 1H),
4.70 (t, J = 9.6 Hz, 1H), 4.63 (d, J = 12.0 Hz, 1H), 4.41 (s, 1H), 4.44-4.40
(m, 1H), 4.26-4.20 (m, 4H), 3.78 (s, 3H), 3.71-3.66 (m, 1H), 3.51 (s, 2H),
3.45 (d, J = 12.6 Hz, 1H), 3.16 (dd, J = 12.6, 3.6 Hz, 1H), 2.27-2.10 (m,
3H), 1.88 (d, J = 10.2 Hz, 3H), 1.38-1.36 (m, 3H), 0.44-0.41 (m, 3H); 13C NMR (150 MHz, CDCl3) δ 178.1, 178.0, 176.3, 174.7, 174.6, 174.0,
173.9, 173.8, 157.9, 145.1, 136.7, 130.3, 130.2, 128.7, 128.7, 128.4,
127.3, 124.8, 114.3, 96.2, 96.2, 78.2, 78.1, 77.8, 70, 70, 60.9, 59.4, 55.3,
53.6, 53.3, 49.4, 49.2, 41.4, 34.2, 31.2, 37.3, 27.2, 21.8, 17.4, 16.8, 16.6; HRMS (ESI-TOF) m/z calcd for C38H50N8O12 + H+: 811.3621 [M+H]+;
found: 811.3640.
Compound 11. A mixture of 10 (7.0 mg, 0.009 mmol), Pd(OH)2/C (3.5 mg) and AcOH (5.2 μL, 0.09 mmol) in MeOH (0.90 mL) was stirred under hydrogen (80 psi). After 24 h, the reaction was filtered through a pad of celite, and then concentrated. The residue was purified by cc (n- PrOH/H2O = 20:1 to 5:1, silica gel) to give 11 (3.5 mg, 0.005 mmol, 56% yields) as a white solid; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.25β) δ 7.86-7.84 (m, 1H), 7.16-7.14 (m, 2H), 6.89 (d, J = 8.4 Hz, 2H), 5.20 (d,
J = 3.2 Hz, 1H), 4.43-4.37 (m, 2H), 4.23-4.03 (m, 4H), 3.77-3.68 (m, 4H),
3.49-3.42 (m, 3H), 3.18-3.14 (m, 1H), 2.21-2.12 (m, 2H), 2.07-1.99 (m,
1H), 1.91-1.90 (m, 3H), 1.85-1.81 (m, 1H), 1.36-1.33 (m, 3H), 0.41-0.36
(m, 3H). 13C NMR (150 MHz, D2O) δ 178.6, 177.5, 175.2, 174.5, 173.4,
160.1, 131.2, 128.8, 126.3, 126.1, 115.0, 92.9, 78.7, 78.6, 78.2, 71.1,
62.9, 61.5, 56.2, 55.7, 50.5, 42.8, 35.8, 33.0, 32.7, 30.7, 30.3, 29.9, 23.7,
22.8, 18.5, 18.4, 17.8, 14.5; HRMS (ESI-TOF) m/z calcd for C28H39N7O11
+ H+: 721.3151 [M+H]+; found: 721.3162.
Compound 12. The reaction was carried out as described above in 10, followed the reaction which was carried out as 11. The final product 12 (8.0 mg, 0.011mmol, 33% over three steps) was obtained from 4- (Trifluoromethyl)phenylacetic acid; 1H NMR (600 MHz, D2O) δ 8.15-8.01 (m, 1H), 7.75-7.60 (m, 2H), 7.55-7.44 (m, 2H), 5.29 (s, 1H), 4.62-4.49 (m,
4H), 4.95-4.27 (m, 7H), 3.78-3.66 (m, 6H), 3.51 (d, J =11.9 Hz, 1H), 3.23-
3.21 (m, 2H), 2.91-2.87 (m, 1H), 2.27-1.98 (m, 2H), 1.91-1.90 (m, 1H),
1.43-1.41 (m, 6H), 0.45-0.42 (m, 3H); 13C NMR (150 MHz, D2O) δ 178.2,
174.6, 174.5, 173.9, 173.7, 173.5, 139, 129.5, 129.5, 128.7, 128.6, 125.6,
91.3, 78.1, 77.6, 70.1, 69.5, 61.0, 59.6, 54.5, 54.3, 54.1, 49.5, 42, 34.6,
34.2, 31.4, 27.9, 22.0, 21.9, 21.8, 20.0, 20.0, 17.3, 16.9; HRMS (ESI-
TOF) m/z calcd for C31H41F3N8O11 + H+: 759.2920 [M+H]+; found: 759.2932.
Compound 13. N-methylpropargylamine (8.4 μL, 0.099 mmol), CuSO4(aq)
(1.0 M, 3.3 μL, 0.0033 mmol) and sodium ascorbate(aq) (1.0 M, 9.9 μL, 0.0099 mmol) was added to the solution of 8 (20 mg, 0.033 mmol) in MeCN/H2O (0.33 mL, v/v = 1:1). The reaction mixture was stirred at 80 °C. After 24 h, the reaction mixture was concentrated to give the residue, followed the reaction which was carried out as described above in 11. The final product 13 (10 mg, 0.017 mmol, 43% over two steps) was obtained; 1H NMR (600 MHz, D2O) δ 8.62-8.41 (m, 1H), 5.27 (s, 1H), 4.74-4.71 (m, 1H), 5.05-4.89 (m, 2H), 4.40-3.91 (m, 9H), 3.64-3.62 (m,
1H), 3.40-3.39 (m, 1H), 3.08-2.90 (m, 2H), 2.86-2.83 (m, 3H), 2.36-2.12
(m, 3H), 2.12-2.09 (m, 2H), 1.99 (s, 3H), 1.93-1.87 (m, 2H), 1.42 (s, 3H), 1.41 (s, 3H), 0.76-0.74 (m, 3H); 13C NMR (150 MHz, D2O) δ 178.5, 178.3,
177.6, 177.4, 173.9, 173.6, 149.7, 94.7, 91.3, 89.6, 77.5, 69.5, 69.2, 68.4,
67.6, 64.4, 62.9, 59.8, 54.5, 54.4, 52, 50.7, 49.4, 49.3, 41.5, 41.4, 31.5,
31.4, 27.8, 27.6, 23.2, 22.0, 21.8, 19.5, 17.4, 17.3, 16.9, 16.8, 16.7, 16.5; HRMS (ESI-TOF) m/z calcd for C23H38N8O10 + H+: 587.2784 [M+H]+;
found: 587.2795.
Compound 14. The reaction was carried out as described above in 13. The final product 14 (13 mg, 0.020 mmol, 48% over two steps) was obtained from 1-methoxy-3-(propyl-2-yn-1-yl)benzene; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.60β) δ 8.54 (s, 1H), 7.43-7.38 (m, 3H),
7.01 (d, J = 7.3 Hz, 1H), 5.25 (d, J = 3.4 Hz, 1H), 4.11-4.09 (m, 1H),
3.87-3.84 (m, 4H), 3.72-3.68 (m, 1H), 3.59-3.54 (m, 1H), 3.36-3.33 (m,
1H), 2.18-2.07 (m, 2H), 2.04-1.98 (m, 1H), 1.92 (s, 3H), 1.81-1.76 (m,
1H), 1.36-1.33 (m, 3H), 0.61-0.57 (m, 3H); 13C NMR (150 MHz, D2O) δ
178.3, 174.8, 173.81, 159.5, 130.7, 118.6, 114.8, 111.1, 91.4, 78.0, 77.5,
69.6, 61.2, 59.8, 55.5, 54.3, 54.2, 50.5, 49.7, 31.3, 27.8, 22.1, 21.9, 17.3,
16.8, 16.1; HRMS (ESI-TOF) m/z calcd for C28H40N7O11 + H+: 650.2780 [M+H]+; found: 650.2790.
Compound 18. A mixture of 15 (1.5 eq), dipeptide S1 (1.0 eq), HBTU (2.0 eq), DIPEA (3.0 eq) was stirred in CH2Cl2 at rt. After 8 h, the reaction was washed with 1.0 N HCl(aq), sat. NaHCO3(aq), and water, subsequently. The organic layer was collected, dried over magnesium sulphate, and purified by cc (CH2Cl2/MeOH = 70:1, silica gel) to give a fully-protected MDP. The MDP was dissolved in the solution of CH2Cl2/TFA (v/v = 3:1), and stirred at 0 ºC. After 30 min, the reaction mixture was concentrated to get residue. A resuspension of the residue, Pd(OH)2 /C (20% w/w), and AcOH was stirred under hydrogen gas (80 psi). After 16 h, the reaction mixture was filtered through a pad of celite, and the filtrate was concentrated. Subsequently, the crude product was purified by cc to afford the final compound 18 (180 mg, 36% over 3 steps); 1H NMR (600 MHz, CD3OD) (Anomers-1.00α : 0.30β) δ 5.16 (d, J = 3.2 Hz, 1H), 4.45-
4.35 (m, 3H), 4.19-4.16 (m, 2H), 3.85 (dd, J = 10.4, 3.2 Hz, 1H), 3.82-
3.67 (m, 4H), 3.50-3.44 (m, 1H), 2.36-2.35 (m, 2H), 2.22-2.14 (m, 1H),
1.96-1.93 (m, 4H), 1.41-1.37 (m, 6H), 1.27 (t, J = 7.1 Hz, 3H); 13C NMR (150 MHz, CD3OD) δ 176.6, 176.3, 174.8, 174.5, 173.74, 173.71, 173.2,
172.1, 171.7, 96.0, 91.0, 81.4, 78.6, 76.9, 76.7, 76.5, 71.8, 70.4, 70.1,
61.3, 61.2, 61.1, 61.0, 56.7, 54.2, 52.22, 52.20, 49.0, 48.9, 30.8, 26.6,
26.3, 21.7, 21.5, 20.0, 18.3, 18.2, 17.0, 16.9, 13.1; HRMS (ESI-TOF) m/z
calcd for C21H35N3O12 + Na+: 544.2113 [M+Na]+; found: 544.2121.
Compound 19. The reaction was carried out as described above in 18. The final product, 19 (160 mg, 29% over 3 steps) was obtained from S16; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.50β) δ 5.15 (d, J = 3.5 Hz,
1H), 4.44-4.41 (m, 1H), 4.31-4.25 (m, 2H), 4.22-4.13 (m, 4H), 3.95 (dd, J
= 10.5, 3.5 Hz, 1H), 3.88-3.67 (m, 3H), 3.59-3.45 (m, 2H), 2.49-2.41 (m,
2H), 2.26-2.20 (m, 1H), 2.01-1.96 (m, 4H), 1.43-1.41 (m, 3H), 1.38-1.36 (m, 3H), 1.24 (q, J = 14.7, 7.3 Hz, 6H); 13C NMR (150 MHz, D2O) δ 175.7,
175.4, 175.04, 175.02, 174.9, 174.2, 173.9, 172.9, 94.9, 90.9, 82.5, 79.5,
78.0, 77.7, 75.7, 71.4, 68.9, 68.7, 62.7, 61.8, 60.6, 60.4, 56.1, 53.7, 51.9,
49.6, 49.5, 46.1, 46.0, 30.1, 25.94, 25.90, 25.6, 22.2, 21.9, 18.6, 16.7,
13.3, 13.2; HRMS (ESI-TOF) m/z calcd for C23H39N3O12 + Na+: 572.2426 [M+Na]+; found: 572.2428.
Compound 20. Lithium hydroxide (2.0 N) was added to the solution of 19 in THF. After stirring for 1 h, the mixture was neutralized with Dowex, filtered, and concentrated. The crude product was purified by cc to afford 20 (29 mg, 34%) as a white solid; 1H NMR (600 MHz, D2O) (Anomers- 1.00α : 0.60β) δ 5.14 (d, J = 3.5 Hz, 1H), 4.31-4.19 (m, 3H), 3.94 (dd, J =
10.5, 3.5 Hz, 1H), 3.92-3.68 (m, 3H), 3.58-3.45 (m, 2H), 2.30-2.23 (m,
2H), 2.13-2.05 (m, 1H), 1.95 (s, 3H), 1.91-1.85 (m, 1H), 1.43-1.41 (m,
3H), 1.38-1.36 (m, 3H). 13C NMR (150 MHz, D2O) δ 179.8, 177.9, 175.7,
173.9, 173.2, 94.9, 90.9, 82.4, 79.4, 78.0, 77.7, 75.7, 71.4, 68.9, 68.7,
66.3, 60.6, 60.4, 56.1, 53.7, 52.3, 49.54, 49.50, 30.8, 29.7, 25.94, 25.91,
22.2, 22.0, 21.9, 18.6, 18.4, 16.77, 16.76, 12.8; HRMS (ESI-TOF) m/z
calcd for C23H39N3O12 + Na+: 572.2426 [M+Na]+; found: 572.2425.
Compound 25. The reaction was carried out as described above in 18. The final product, 25 (20 mg, 14% over 3 steps) was obtained from S9;
1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.47β) δ 5.16 (d, J = 3.5 Hz,
0.64H), 4.66 (d, J = 8.5 Hz, 0.30H), 4.46 – 4.42 (m, 3H), 4.32 – 4.22 (m,
2H), 3.95 – 3.48 (m, 8H), 2.36 – 2.33 (m, 2H), 2.21 – 2.19 (m, 1H), 2.02 –
1.97 (m, 4H), 1.43 (dd, J = 7.3, 4.4 Hz, 3H), 1.37 (t, J = 6.1 Hz, 3H); 13C
NMR (150 MHz, D2O) δ 179.62, 179.58, 175.7, 175.4, 175.0, 174.2,
174.0, 172.7, 94.9, 90.8, 82.4, 79.4, 78.0, 77.7, 75.7, 71.5, 69.0, 68.7,
65.6, 60.4, 56.1, 53.7, 52.49, 52.47, 49.54, 49.50, 41.8, 32.1, 26.5, 26.4,
22.2, 21.9, 18.6, 16.8, 16.5; HRMS (ESI-TOF) m/z calcd for C H ClN O + H+: 556.1904 [M+H]+; found: 556.1905.
Compound 21. The reaction was carried out as described above in 18. The final product, 21 (58 mg, 40% over 3 steps) was obtained from S14; 1H NMR (600 MHz, CD3OD) (Anomers-1.00α : 0.20β) δ 5.16 (d, J = 3.4 Hz, 1H), 4.39-4.33 (m, 2H), 4.29-4.26 (m, 1H), 4.13 (q, J = 7.1 Hz, 2H)
3.87 (dd, J = 10.4, 3.2 Hz, 1H), 3.82-3.78 (m, 2H), 3.72 (dd, J = 11.9, 5.2
Hz, 1H), 3.63 (dd, J = 10.4, 8.9 Hz, 1H), 3.49 (t, J = 9.5 Hz, 1H), 2.43-
2.40 (m, 2H), 2.25-2.10 (m, 1H), 1.95-1.88 (m, 4H), 1.40-1.38 (m, 6H),
1.25 (t, J = 7.1 Hz, 3H); 13C NMR (150 MHz, CD3OD) δ 175.2, 174.9,
174.0, 173.0, 172.1, 91.0, 79.0, 76.7, 71.8, 70.2, 60.3, 54.1, 52.3, 49.4,
30.1, 26.5, 21.5, 18.3, 16.3, 13.1; HRMS (ESI-TOF) m/z calcd for C21H36N4O11 + Na+: 543.2273 [M+Na]+; found: 543.2289.
Compound 22. The reaction was carried out as described above in 18. The final product, 22 (94 mg. 31% over 3 steps) was obtained from S15; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.50β) δ 5.18 (d, J = 3.5 Hz,
1H), 4.34-4.19 (m, 4H), 3.98 (dd, J = 10.5, 3.5 Hz, 1H), 3.90-3.71 (m, 4H),
3.62-3.50 (m, 2H), 2.35-2.32 (m, 2H), 2.16-2.06 (m, 1H), 2.00-1.94 (m,
4H), 1.46-1.39 (m, 6H); 13C NMR (150 MHz, D2O) δ 178.6, 177.7, 175.8,
175.6, 174.2, 174.1, 173.99., 173.96, 94.9, 90.9, 82.5, 79.6, 79.5, 78.1,
77.8, 75.7, 71.5, 69.0, 68.8, 60.7, 60.5, 56.1, 54.5, 54.3, 53.7, 49.6, 49.5,
31.52, 31.50, 27.8, 22.2, 22.0, 18.7, 18.6, 16.8, 16.5; HRMS (ESI-TOF)
m/z calcd for C19H32N4O11 + Na+: 515.1960 [M+Na]+; found: 515.1944.
Compound 26. The reaction was carried out as described above in 18. The final product, 26 (40 mg, 35% over 3 steps) was obtained from S7; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.48β) δ 5.16 (d, J = 3.5 Hz,
0.63H), 4.66 (d, J = 8.5 Hz, 0.30H), 4.35 – 4.22 (m, 3H), 3.95 – 3.49 (m,
6H), 2.38 – 2.28 (m, 2H), 2.21 – 2.10 (m, 1H), 2.06 – 1.92 (m, 4H), 1.85 –
1.75 (m, 2H), 1.74 – 1.61 (m, 2H), 1.53 – 1.45 (m, 3H), 1.42 (dd, J = 7.2,
4.1 Hz, 3H), 1.40 – 1.24 (m, 6H). 13C NMR (150 MHz, D2O) δ 179.5,
179.4, 175.6, 175.3, 174.9, 174.2, 173.9, 172.8, 94.9, 90.8, 82.3, 79.3,
78.0, 77.6, 75.7, 75.3, 71.5, 69.0, 68.7, 60.6, 60.4, 56.1, 53.7, 53.0,
52.89, 52.87, 49.5, 49.4, 49.0, 32.4, 31.9, 30.69, 30.65, 30.61, 26.6, 26.4,
26.3, 24.7, 22.9, 22.8, 22.2, 21.9, 18.59, 18.57, 16.8, 16.5; HRMS (ESI- TOF) m/z calcd for C25H41N3O12 + H+: 576.2763 [M+H]+; found: 576.2761.
Compound 27. The reaction was carried out as described above in 18. The final product, 27 (32 mg, 21% over 3 steps) was obtained from S8. 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.51β) 7.36 – 7.23 (m, 5H), δ
5.15 (d, J = 3.5 Hz, 0.63H), 4.64 (d, J = 8.4 Hz, 0.32H), 4.43 – 4.37 (m,
1H), 4.38 – 4.32 (m, 2H), 4.31 – 4.18 (m, 2H), 3.98 – 3.41 (m, 6H), 2.94
(t, J = 6.4 Hz, 2H), 2.25 (t, J = 7.4 Hz, 2H), 2.06 – 1.97 (m, 1H), 1.93 (d, J
= 4.7 Hz, 3H), 1.88 – 1.74 (m, 1H), 1.36 (dd, J = 6.2, 5.6 Hz, 6H); 13C
NMR (150 MHz, D2O) δ 176.91, 176.88, 175.5, 175.3, 174.6, 174.2,
173.9, 172.6, 138.1, 129.0, 128.6, 126.7, 94.9, 90.9, 82.3, 79.4, 78.0,
77.6, 75.7, 71.4, 69.0, 68.7, 66.4, 60.6, 60.5, 56.1, 53.6, 51.9, 49.43,
49.39, 34.1, 29.9, 25.7, 22.2, 21.9, 18.6, 16.8. HRMS (ESI-TOF) m/z
calcd for C H N O + H+: 598.2607 [M+H]+; found: 598.2617.
Compound 23. The reaction was carried out as described above in 18.The final product, 23 (76 mg, 48% over 3 steps) was obtained from S17; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.50β) δ 5.15 (d, J = 3.4 Hz, 1H), 4.55 (t, J = 12.7, 6.4 Hz, 1H), 4.30-4.23 (m, 2H), 3.97 (dd, J =
10.4, 3.4Hz, 1H), 3.91-3.69 (m, 4H), 3.59-3.49 (m, 2H), 2.66 (d, J = 6.4
Hz, 2H), 1.98 (s, 3H), 1.43-1.38 (m, 6H); 13C NMR (150 MHz, D2O) δ
177.7, 176.2, 175.9, 174.61, 174.60, 174.2, 173.9, 94.8, 90.94, 90.92,
82.4, 79.6, 78.01, 78.0, 77.72, 77.71, 75.6, 71.4, 68.8, 68.7, 60.6, 60.5,
56.1, 53.7, 51.0, 49.70, 49.69, 38.3, 22.2, 22.0, 18.7, 18.4; HRMS (ESI-
TOF) m/z calcd for C18H30N4O11 + Na+: 501.1803 [M+Na]+; found: 501.1792.
Compound 24. The reaction was carried out as described above in 18. The final product, 24 (20 mg, 13% over 3 steps) was obtained from S2; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.50β) δ 5.16 (d, J = 3.5 Hz,
0.6H), 4.66 (d, J = 8.5 Hz, 0.3H), 4.41 (dd, J = 9.2, 5.3 Hz, 1H), 4.33 –
4.20 (m, 2H), 4.16 (t, J = 6.5 Hz, 2H), 3.98 – 3.44 (m, 6H), 2.43 – 2.37 (m,
2H), 2.23 – 2.15 (m, 1H), 2.05 – 1.93 (m, 4H), 1.66 – 1.59 (m, 2H), 1.42
(dd, J = 7.3, 4.3 Hz, 3H), 1.39 – 1.31 (m, 5H), 0.89 (t, J = 7.4 Hz, 3H); 13C NMR (150 MHz, D2O) δ 178.03, 177.99, 175.7, 175.4, 174.9, 174.2,
Compound 28. The reaction was carried out as described above in 18. The final product, 28 (50 mg, 40% over 3 steps) was obtained from S10; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.42β) δ 5.14 (d, J = 3.5 Hz,
0.64H), 4.66 (d, J = 8.5 Hz, 0.27H), 4.32 – 4.07 (m, 3H), 4.00 – 3.44 (m,
6H), 3.25 – 3.12 (m, 2H), 2.48 – 2.40 (m, 2H), 2.18 – 2.09 (m, 1H), 2.00 –
1.89 (m, 4H), 1.49 – 1.43 (m, 2H), 1.41 (dd, J = 7.2, 4.1 Hz, 3H), 1.37 (dd,
J = 6.8, 4.4 Hz, 3H), 1.31 – 1.23 (m, 2H), 0.86 (t, J = 7.4 Hz, 3H); 13C
NMR (150 MHz, D2O) δ 178.8, 175.8, 175.6, 175.0, 174.9, 174.2, 173.9,
173.1, 173.0, 94.9, 90.9, 82.5, 79.6, 78.1, 77.7, 75.7, 71.4, 68.9, 68.6,
60.6, 60.4, 56.1, 54.3, 53.7, 53.6, 53.55, 53.51, 49.7, 42.5, 39.2, 39.1,
31.5, 30.4, 26.8, 26.78, 22.1, 21.9, 19.33, 19.28, 18.6, 17.7, 16.6, 16.2,
12.9, 12.1; HRMS (ESI-TOF) m/z calcd for C23H40N4O11 + H+: 549.2766 [M+H]+; found: 549.2770.
Compound 29. The reaction was carried out as described above in 18. The final product, 29 (45 mg, 34% over 3 steps) was obtained from S11; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.50β) δ 5.15 (d, J = 3.5 Hz,
0.62H), 4.67 (d, J = 8.5 Hz, 0.31H), 4.32 – 4.07 (m, 3H), 4.01 – 3.44 (m,
6H), 3.25 – 3.11 (m, 2H), 2.41 – 2.30 (m, 2H), 2.16 – 2.05 (m, 1H), 2.00 –
1.87 (m, 3H), 1.52 – 1.45 (m, 2H), 1.42 (dd, J = 7.2, 3.8 Hz, 3H), 1.37 (dd,
J = 6.8, 4.6 Hz, 3H), 1.31 – 1.19 (m, 6H), 0.88 – 0.81 (m, 3H); 13C NMR
(150 MHz, D2O) δ 178.8, 175.8, 175.6, 174.94, 174.91, 174.2, 173.9,
172.9, 94.9, 90.9, 82.5, 79.6, 78.1, 77.7, 75.7, 71.4, 68.9, 68.7, 60.6,
60.4, 56.1, 53.8, 53.6, 53.5, 49.7, 49.0, 39.4, 31.6, 30.6, 28.2, 26.8,
25.63, 25.56, 22.1, 21.9, 21.8, 18.62, 18.61, 16.58, 16.56, 16.5, 13.3; HRMS (ESI-TOF) m/z calcd for C25H44N4O11 + H+: 577.3079 [M+H]+;
found: 577.3088.
Compound 30. The reaction was carried out as described above in 18. The final product, 30 (30 mg, 25% over 3 steps) was obtained from S13; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.52β) δ 5.15 (d, J = 3.5 Hz,
0.62H), 4.66 (d, J = 8.5 Hz, 0.32H), 4.31 – 4.17 (m, 3H), 3.99 – 3.44 (m,
7H), 2.48 – 2.36 (m, 2H), 2.15 – 2.05 (m, 1H), 1.99 – 1.90 (m, 4H), 1.84 –
1.74 (m, 2H), 1.74 – 1.63 (m, 2H), 1.61 – 1.53 (m, 1H), 1.43 – 1.39 (m,
3H), 1.39 – 1.34 (m, 3H), 1.36 – 1.02 (m, 5H); 13C NMR (150 MHz, D2O)
δ 177.38, 177.36, 175.8, 175.6, 174.94, 174.92, 174.2, 173.9, 171.7,
94.9, 90.9, 82.5, 79.7, 78.1, 77.7, 75.7, 71.4, 68.8, 68.6, 60.6, 60.4, 56.1,
53.7, 53.2, 49.69, 49.66, 49.1, 31.8, 30.4, 26.4, 24.8, 24.4, 24.37, 22.2,
21.9, 18.6, 16.5; HRMS (ESI-TOF) m/z calcd for C25H42N4O11 + H+:
575.2923 [M+H]+; found: 575.2938.
Compound 31. The reaction was carried out as described above in 18. The final product, 31 (40 mg, 15% over 3 steps) was obtained from S12; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.49β) δ 5.15 (d, J = 3.5 Hz,
0.57H), 4.67 (d, J = 8.5 Hz, 0.28H), 4.41 (dd, J = 9.4, 5.2 Hz, 1H), 4.31 –
4.18 (m, 2H), 4.09 – 3.43 (m, 8H), 2.51 – 2.40 (m, 2H), 2.25 – 2.09 (m,
1H), 2.05 – 1.92 (m, 4H), 1.42 (dd, J = 7.3, 4.3 Hz, 3H), 1.37 (dd, J = 6.8,
4.8 Hz, 3H); 13C NMR (150 MHz, D2O) δ 177.07, 177.05, 175.8, 175.6,
175.0, 174.2, 174.0, 173.9, 163.4, 163.1, 162.9, 162.6, 119.2, 117.3,
115.3, 113.4, 94.9, 90.9, 82.5, 79.6, 78.1, 77.7, 75.7, 71.4, 68.8, 68.6,
60.6, 60.4, 56.1, 53.7, 53.0, 49.6, 38.6, 38.4, 38.2, 30.0, 26.1, 22.1, 21.9,
18.6, 16.6; HRMS (ESI-TOF) m/z calcd for C22H33F5N4O11 + H+: 625.2139 [M+H]+; found: 625.2131.
Compound 32. The reaction was carried out as described above in 18. The final product, 32 (63 mg, 17% over 3 steps) was obtained from S3; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.53β) δ 5.16 (d, J = 3.5 Hz,
0.66H), 4.66 (d, J = 8.4 Hz, 0.35H), 4.38 (dd, J = 9.0, 5.1 Hz, 1H), 4.35 –
4.21 (m, 2H), 4.20 – 4.09 (m, 2H), 3.98 – 3.43 (m, 6H), 2.34 – 2.25 (m,
2H), 2.20 – 2.10 (m, 1H), 1.69 – 1.60 (m, 2H), 1.42 (dd, J = 7.3, 4.1 Hz,
3H), 1.37 (t, J = 6.1 Hz, 3H), 1.35 – 1.21 (m, 10H), 0.84 (t, J = 6.5 Hz,
3H); 13C NMR (150 MHz, D2O) δ 179.74, 179.71, 175.5, 175.2, 174.72,
174.69, 174.2, 173.9, 173.2, 94.9, 90.8, 82.3, 79.3, 78.0, 77.6, 75.7, 71.5,
69.1, 68.8, 66.32, 66.29, 60.7, 60.5, 56.1, 53.7, 52.6, 52.6, 49.51, 49.46,
32.4, 31.2, 28.5, 28.4, 27.8, 26.8, 26.7, 25.2, 22.2, 22.1, 22.0, 18.6, 16.9,
13.5; HRMS (ESI-TOF) m/z calcd for C27H47N3O12 + Na+: 628.3052 [M+Na]+; found: 628.3057.
Compound 33. The reaction was carried out as described above in 18. The final product, 33 (124 mg, 43% over 3 steps) was obtained from S4; 1H NMR (600 MHz, D2O) (Anomers-1.00α : 0.36β) δ 5.16 (d, J = 3.5 Hz,
0.70H), , 4.66 (d, J = 8.4 Hz, 0.25H), 4.52 – 4.44 (m, 1H), 4.39 – 4.20 (m,
2H), 4.17 – 4.03 (m, 2H), 4.00 – 3.41 (m, 6H), 2.39 (t, J = 7.4 Hz, 2H),
2.21 – 2.11 (m, 1H), 2.02 – 1.92 (m, 4H), 1.67 – 1.58 (m, 2H), 1.42 (t, J =
6.0 Hz, 3H), 1.37 (t, J = 5.5 Hz, 3H), 1.35 – 1.18 (m, 18H), 0.86 (t, J = 6.7
Hz, 3H); 13C NMR (150 MHz, D2O) δ 175.9, 175.8, 175.3, 175.1, 174.2,
174.1, 174.0, 173.6, 172.2, 95.0, 90.9, 82.4, 79.6, 78.0, 77.6, 75.8, 71.5,
69.1, 68.9, 68.8, 65.7, 61.7, 60.8, 60.7, 60.4, 56.2, 56.0, 53.6, 53.4, 51.7,
49.6, 49.4, 32.0, 29.9, 29.8, 29.7, 29.5, 28.3, 26.2, 25.8, 22.6, 22.3, 22.1,
18.8, 18.6, 17.2, 16.8, 13.8; HRMS (ESI-TOF) m/z calcd for C31H55N3O12
+ Na+: 684.3678 [M+Na]+; found: 684.3685.
Compound 34. The reaction was carried out as described above in 18. The final product, 34 (32 mg, 19% over 3 steps) was obtained from S5; 1H NMR (600 MHz, CD3OD) (Anomers-1.00α : 0.34β) δ 5.14 (d, J = 3.4 Hz, 0.70H), 4.55 (d, J = 8.3 Hz, 0.24H), 4.48 – 4.32 (m, 3H), 4.17 – 4.06
(m, 2H), 3.93 – 3.40 (m, 6H), 2.38 (t, J = 7.3 Hz, 2H), 2.24 – 2.14 (m, 1H),
2.00 – 1.93 (m, 4H), 1.70 – 1.61 (m, 2H), 1.41 – 1.37 (m, 6H), 1.33 –
1.23 (m, 26H), 0.90 (t, J = 6.9 Hz, 3H); 13C NMR (150 MHz, CD3OD) δ
177.0, 176.3, 176.0, 175.2, 174.6, 173.6, 173.2, 97.5, 92.6, 83.1, 80.4,
78.5, 78.4, 78.1, 73.4, 71.8, 71.6, 66.7, 66.7, 62.9, 62.8, 58.3, 55.7, 53.5,
53.5, 50.5, 50.4, 33.2, 31.6, 31.0, 30.9, 30.9, 30.8, 30.6, 30.5, 29.8, 28.0,
27.8, 27.1, 23.9, 23.3, 23.0, 19.8, 19.8, 18.6, 18.5, 14.6; HRMS (ESI- TOF) m/z calcd for C35H63N3O12 + H+: 718.4485 [M+H]+; found: 718.4456.
Compound 35. The reaction was carried out as described above in 18. The final product, 35 (20 mg, 14% over 3 steps) was obtained from S6; 1H NMR (600 MHz, CD3OD) (Anomers-1.00α : 0.28β) δ 5.16 (d, J = 3.4 Hz, 0.78H), 4.55 (d, J = 8.0 Hz, 0.22H), 4.48 – 4.31 (m, 3H), 4.20 – 4.05
(m, 2H), 3.94 – 3.40 (m, 6H), 2.44 – 2.31 (m, 2H), 2.26 – 2.12 (m, 1H),
2.06 – 1.89 (m, 4H), 1.72 – 1.59 (m, 2H), 1.39 (t, J = 7.8 Hz, 6H), 1.37 –
1.14 (m, 34H), 0.90 (t, J = 6.9 Hz, 3H); 13C NMR (150 MHz, CD3OD) δ
177.4, 176.2, 175.9, 175.1, 174.6, 173.5, 173.1, 97.4, 92.4, 82.8, 80.0,
78.3, 78.2, 77.9, 73.2, 71.8, 71.5, 66.5, 66.5, 62.7, 62.7, 58.2, 55.6, 53.5,
50.4, 33.1, 31.8, 30.8, 30.7, 30.5, 30.4, 29.7, 28.1, 27.9, 27.7, 27.0, 23.7,
23.1, 22.9, 19.7, 19.6, 18.4, 18.3, 14.4; HRMS (ESI-TOF) m/z calcd for C39H71N3O12 + Na+: 796.4930 [M+Na]+; found: 796.4927.Me
Measurement of NF-κB Transcriptional Activity
HEK-BlueTM hNOD2 Cells (Invivogen; San Diego, CA, U.S.) were cultured in accordance with the manufacturer’s instructions. HEK-BlueTM hNOD2 Cells was assayed for NF-κB transcriptional activity changes upon incubation (3.6 × 106 cells/mL) with MDP and other NOD2 agonistic compounds (10-1000 nM) for 16 h. Secreted embryonic alkaline phosphatase (SEAP) activity was determined in the supernatant in accordance with the manufacturer’s instructions. An amount of 20 μL of SEAP-inducer compound or negative control was added to 180 μL of cells in HEK-BlueTM Detection medium and incubated at 37 °C for 16 h. Absorbance was measured on a M5 microplate reader (Reading, U.K.) at 640 nm.
Statistics
All experiments were performed at least three times, with average values expressed as the mean ± SD. Statistical significance was determined by the Dunnet multiple comparison test. Differences were considered significant for p < 0.05 and highly significant for p < 0.01.
Computation Method
To understand the binding mode of 1 and 33 in NOD2LRR, molecular docking was performed using AutoDock Vina.38 We used rabbit NOD2 (rNOD2) crystal structure (PDBID: 5IRN)34 as macromolecule, and 3D coordinates of 1 and 33 (generated by Chem3D) as ligands. Prior to docking, the polar hydrogens were added to rNOD2LRR. Kollman charges were assigned to rNOD2LRR, Muramyl dipeptide and Gasteiger partial charges were applied to ligands (1 and 33) using AutoDock Tools-1.5.6.39 Based on previous studies,23,35,36 the concave surface of NOD2LRR was considered as binding site. PyMOL (www.pymol.org) and LigPlot+ 2.140 was used for interaction study and visualization.