One-pot synthesis and antifungal activity against plant pathogens of quinazolinone derivatives containing an amide moiety

Bioorganic & Medicinal Chemistry Letters xxx (2016) xxx–xxx

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One-pot synthesis and antifungal activity against plant pathogens of quinazolinone derivatives containing an amide moiety Jin Zhang a,b, Jia Liu a, Yangmin Ma a,b,⇑, Decheng Ren a, Pei Cheng a, Jiawen Zhao a, Fan Zhang a, Yuan Yao c a

College of Chemistry & Chemical Engineering, Shaanxi University of Science & Technology, Xi’an 710021, PR China Key Laboratory of Auxiliary Chemistry & Technology for Chemical Industry, Ministry of Education, Xi’an 710021, PR China c Institute of Theoretical and Simulational Chemistry, Academy of Fundamental and Interdisciplinary Science, Harbin Institute of Technology, Harbin 150080, PR China b

a r t i c l e

i n f o

Article history: Received 9 December 2015 Revised 26 February 2016 Accepted 14 March 2016 Available online xxxx Keywords: 3-Acylamino substituted quinazolinones CeO2 nanoparticles Phytopathogenic fungi Structure–activity relationship Molecular docking

a b s t r a c t An efficient one-pot, three-component synthesis of quinazolinone derivatives containing 3-acrylamino motif was carried out using CeO2 nanoparticles as catalyst. Thirty-nine synthesized compounds were obtained with satisfied yield and elucidated by spectroscopic analysis. Four phytopathogenic fungi were chosen to test the antifungal activities by minimum inhibitory concentration (MIC) method. Compounds 4ag, 4bb, 4bc showed broad antifungal activities against at least three fungi, and dramatic effects of substituents on the activities were observed. Docking studies were established to explore the potential antifungal mechanism of quinazolinone derivatives as the chitinase inhibitors, and also verified the importance of the amide moiety. Ó 2016 Elsevier Ltd. All rights reserved.

The management of plant diseases caused by phytopathogenic fungi1 was highly important for preventing the losses in agricultural economy2 and toxins produced by plant pathogens.3 Nowadays, various commercial plant fungicides, such as carbendazim, metalaxyl, isoprothiolane, triadimefon, thiabendazole, benomyl, thiophanate methyl, have been applied in effective control of the fungal plant diseases in current agricultural system. However, many drawbacks have emerged with wide using of these fungicides, such as the increase of the fungal resistance4 and fungicide residues, which were harmful to humans and animals.5,6 Recently, there were three ways to the further discovery and development of the novel antifungal lead molecules7: the computational screening techniques for new inhibitors to the certain protein,8 the new compounds obtained from natural products,9,10 and the commonly used chemical scaffolds with biological activities.11–13 Quinazolinone is one of the common chemical scaffolds, which belongs to a family of heterocyclic nitrogen compounds. It plays an important role in medicinal chemistry and has a variety of biological activities, such as antitumor, anti-inflammatory, antiviral and antifungal.14,15 Because of the significant value in pharmaceuticals, the synthesis of quinazolinone and its derivatives have attracted considerable interests. In general, the condensation reaction of isatoic anhydride, primary amine or ammonium salts with aldehydes was widely employed. It was catalyzed by

⇑ Corresponding author.

b-cyclodextrin-SO3H,16 nanoparticles,17,18 Saccharomyces cerevisiae (baker’s yeast),19 montmorillonite K10,20 cation-exchange resin,21 palladium,22 ionic liquid-water.23 A vast number of quinazolinone derivatives have been designed to provide effective drugs, especially, some antifungal agents, such as tryptanthrin24,25 and 2-acetylquinazolin-4(3H)-one (Fig. 1).26,27 In our previous work, dihydroquinazolin-4(1H)-one derivatives have been found to be potent anti-bacterial compounds.28 Typically, the amide moiety was an important fragment of antifungal molecules, which could increase the activities in vitro.29–32 Inspired by these studies, we initiated a study to synthesized quinazolinone derivatives containing amide moiety with three rings (ring A, B and C) in the 3-acylaminoquinazolin-4(1H)-one structure (Fig. 1) as antifungal agents used for plant protection. To make the synthetic process more convenient, heterogeneous catalysts was introduced in this study. Cerium(IV) oxide (CeO2) nanoparticles were first conducted in the efficient one-pot synthesis of 3-acylaminoquinazolin-4(1H)-one derivatives. As a green and heterogeneous catalyst, CeO2 can be used in a broad range of organic reactions,33,34 such as the catalytic CO2 conversion to organic carbonates in alcohol,35 construction of amide bonds36 and alcoholysis of amides.37 The vitro antifungal activities were tested against four phytopathogenic fungi, including Phytophthora capsici, Colletotrichum gloeosporioides, Valsa mali Miyabe et Yamada, and Alternaria alternate. In order to illustrate the theoretically antifungal mechanism, family 18 chitinase38 was chosen for the molecular studies

http://dx.doi.org/10.1016/j.bmcl.2016.03.052 0960-894X/Ó 2016 Elsevier Ltd. All rights reserved.

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J. Zhang et al. / Bioorg. Med. Chem. Lett. xxx (2016) xxx–xxx Table 1 Optimization of reaction conditions and quantity of catalysts for the synthesis of compound 4aaa

Figure 1. Reported quinazolinone antifungal agents form natural or synthesis and designed target compounds.

for the broad antifungal activities of synthesized compounds. It was one of the important enzymes for degrading chitin (polymer of b-(1,4)-linked N-acetylglucosamine) involved in the essential life cycles of pathogenic fungi. Chitin was a major structural component of fungi cell walls and insect cuticles, and it also cannot be found in higher plants and mammals.12,39 The chitinase inhibitors are potential fungicides and have attracted much attention for the low toxicity to non-target organisms and safe to the ecological environment.31,40 The binding modes of the allosamidin and N-acetyl-D-allosamine natural origin to family 18 chitinase were previously determined by X-ray crystallography (PDB:2A3E).41 Due to allosamidin and N-acetyl-D-allosamine42 restricted in use for their high cost and limited availability, the development of new antifungal agents to the same active site in chitinase was crucial. The synthesized compounds contained the analogous nitrogen heterocycle and amide moiety just like the original inhibitors. Thus, we chose family 18 chitinase as the target for the docking study and the result was satisfied with vitro antifungal activities. The structure of 3-acrylaminoquinazolinone was verified to be active toward the target. The docking simulation was performed and explained the special structure played an important role in increasing the binding interaction. In addition, the synthetic method we developed was convenient and efficient for industrial production. Our efforts to synthesize the functionalized quinazolinone derivatives bearing acylamino motif began by exploring the one-pot process of isatoic anhydride, benzhydrazide, and benzaldehyde. Compound 4aa was obtained in yields of 82%, 63%, and 40% by using CeO2 nanoparticles, CuO nanoparticles, and Fe3O4 nanoparticles as the catalyst, respectively (Table 1, entries 1–3). CeO2 nanoparticles appeared more efficient than other nanoparticles. Studies were continued to improve the yields by conducting the reaction in different solvents and catalysed loadings. Aprotic solvents dimethyl formamide(DMF), acetonitrile and dimethylsulfoxide (DMSO) failed to provide the desired products (Table 1, entries 4–6), while methanol and water gave the desired product in moderate yields (Table 1, entries 7, 8). Ethanol was found to be the superior choice for the reaction (Table 1, entry 11). The effect of the amount of catalyst was also investigated (Table 1, entries 9–12). The yield was increased from 57% to 82% by the increasing of the loading amount of CeO2 nanoparticles from 3 mol % to 5 mol %. When the concentration of CeO2 nanoparticles was increased above 5 mol %, the yield was no further improved. Compared with CeO2 powder (Table 1, entry 13), CeO2 nanoparticles provided the higher yield. The best yield (82%) (Table 1, entry 11) was obtained under the optimal condition of refluxing with 5 mol % CeO2 nanoparticles in ethanol. With the optimal conditions, a wide range of functional groups such as electron donating and electron withdrawing group on ring B and ring C were well tolerated (Scheme 1). Thirty-nine 3-acylaminoquinazolinone derivatives (4aa–4ee) were synthesized

Entry

Catalyst

Solvent

Catalyst loading (mol %)

Time (h)

Yieldsb (%)

1 2 3 4 5 6 7 8 9 10 11 12 13

nano nano nano nano nano nano nano nano nano nano nano nano CeO2

EtOH EtOH EtOH DMF Acetonitrile DMSO MeOH H2O EtOH EtOH EtOH EtOH EtOH

10 10 10 10 10 10 10 10 — 8 5 3 10

6 6 6 10 10 10 6 6 10 5 5 5 8

82 63c 40d Trace Trace Trace 70 51 Trace 82 82 57 20e

CeO2 CuO Fe3O4 CeO2 CeO2 CeO2 CeO2 CeO2 CeO2 CeO2 CeO2 CeO2

a All reactions were carried out with 1.5 mmol of isatoic anhydride, 1.6 mmol of benzhydrazide, and 1.6 mmol of benzaldehyde in the presence of catalyst in solvent (5 mL) at refluxing temperature. b Isolated yields. c CuO nanoparticles (Outside Diameter(OD) 40 nm) as catalyst. d Fe3O4 nanoparticles (OD 40 nm) as catalyst. e CeO2 powder as catalyst.

in satisfied yield and listed in Table 2. The substrates with electron-donating groups on the B or C ring, such as OH, OMe, Me, N(CH3)2 and CH(CH3)2, exhibited good reactivity(4ab–4ah, 4bb–4bd, 4ca–4cb, 4da–4de, 4eb–4ed). The strong electronwithdrawing group, NO2 or CHO, led to the corresponding products 4ai–4ak, 4be and 4cc with slightly lower yields. It was notable that heterocyclic aldehydes, such as 3-pyridinecarboxaldehyde, 4-pyridinecarboxaldehyde, and furfural, were also found to be suitable for the reaction and gave the corresponding products in satisfactory yields (Table 2, 4al–4an, 4bf, 4cd, 4ce). In addition, isobutyraldehyde and cyclohexanone also furnished the desired products 4ao, 4ap, 4cf, 4df, 4ee. The structures of all compounds were confirmed by analytical and spectral data. In particular, 17 compounds (4ak, 4am, 4ba–4bf, 4cb–4ce, 4da–4dd, 4df) were first synthesized. A possible formation mechanism of 4 was shown in Scheme 2. CeO2 nanoparticles activate the isatoic anhydride in the protic solvent, followed by nucleophilic attack of phenylhydrazine or benzhydrazide. CO2 was then eliminated, resulting in intermediate I. In the presence of CeO2 nanoparticles, intermediate I was subject to a nucleophilic attack by an aldehyde to form intermediate II. Intermolecular cyclization produced intermediate III, and a 1,5-H shift transforms intermediate III into the final product. All the synthesized compounds were screened for their in vitro antifungal activity against four phytopathogenic fungi (P. capsici, C. gloeosporioides, V. mali, A. alternate). The results showed all the compounds displayed the activity in varying degrees against each of the test fungi (Table 2). Most compounds represented mild activity against each of the fungi at 128 lg/mL. Part of the synthesized compounds appeared the same active with the positive control ketoconazole. Compounds 4ab, 4ac, 4ae, 4bc and 4cb exhibited the highest antifungal activity against P. capsici at 32 lg/mL, and compounds 4ad, 4ag, 4ak, 4al, 4bb–4bd, 4bf, 4cb, 4cc and 4de showed the same activity with the positive control at 32 lg/mL against C. gloeosporioides. Compounds 4af, 4ag, 4bb, 4bf, 4ee appeared the best activities at 32 lg/mL against V. mali which were slightly lower than the positive control. The tested results of compounds 4aa, 4ab, 4ad, 4ag, 4aj, 4am, 4bb, 4bc, 4cd, 4da, 4dc and 4de were as the same MIC values as the positive control at 64 lg/mL against A. alternate. In general, compounds 4ag, 4bb and 4bc presented a broad-spectrum antifungal activity against at least three fungi.

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J. Zhang et al. / Bioorg. Med. Chem. Lett. xxx (2016) xxx–xxx

Scheme 1. The one-pot synthesis route of 3-acylaminoquinazolinone derivatives.

Table 2 Synthesis of different substitution patterns of compounds 4aa–4ee and their antifungal activity Compounds

4aa 4ab 4ac 4ad 4ae 4af 4ag 4ah 4ai 4aj 4ak 4al 4am 4an 4ao 4ap 4ba 4bb 4bc 4bd 4be 4bf 4ca 4cb 4cc 4cd 4ce 4cf 4da 4db 4dc 4dd 4de 4df 4ea 4eb 4ec 4ed 4ee Ketoconazole a

Yieldsa (%)

82 78 79 83 84 76 77 78 51 54 67 76 72 78 69 81 80 81 80 79 71 84 85 88 83 85 88 87 76 76 72 72 73 83 73 73 76 81 66 —

R1

Ph-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COPh-COo-OCH3-Ph-COo-OCH3-Ph-COo-OCH3-Ph-COo-OCH3-Ph-COo-OCH3-Ph-COo-OCH3-Ph-COo-CH3-Ph-COo-CH3-Ph-COo-CH3-Ph-COo-CH3-Ph-COo-CH3-Ph-COo-CH3-Ph-CO3-pyridyl-CO3-pyridyl-CO3-pyridyl-CO3-pyridyl-CO3-pyridyl-CO3-pyridyl-COPhPhPhPhPh—

MIC (lg/mL)

R2

Ph 2-OH-Ph 4-OH-Ph 4-OCH3-Ph 3-MeO-4-HO-C6H3 4-CH(CH3)2-Ph styryl 4-N(CH3)2-Ph 3-NO2-Ph 2-NO2-Ph 4-CHO-Ph 3-pyridyl 4-pyridyl 2-furanyl iPr cyclohexanone Ph 4-OCH3-Ph styryl 4-N(CH3)2-Ph 3-NO2-Ph 3-pyridyl 4-OH-Ph 3-MeO-4-HO-C6H3 3-NO2-Ph 2- pyridyl 4-pyridyl iPr 2-OH-Ph 4-OCH3-Ph 4-CH(CH3)2-Ph 4-N(CH3)2-Ph 3-MeO-4-HO-C6H3 cyclohexanone Ph 2-OH-Ph 4-CH(CH3)2-Ph styryl iPr —

P. capsici

C. gloeosporioides

V. mali

A. alternate

256 32 32 256 32 64 64 128 128 64 128 128 64 128 128 128 128 64 32 128 64 128 64 32 128 128 128 128 128 128 128 128 128 128 128 64 128 128 128 32

128 64 64 32 64 64 32 64 128 128 32 32 128 128 64 128 128 32 32 32 64 32 64 32 32 128 128 128 128 64 64 64 32 64 128 128 128 64 128 32

128 64 128 64 64 32 32 64 128 128 64 64 128 128 64 64 128 32 64 32 128 32 128 128 128 128 128 128 128 64 128 128 64 128 128 128 128 128 32 16

64 64 128 64 128 128 64 128 128 64 128 128 64 128 128 128 128 64 64 128 64 128 256 128 128 64 128 128 64 128 64 128 64 128 128 128 128 128 128 64

Isolated yields.

Comparing the MIC values of various compounds in Table 2, it was observed that the compounds bearing acylamino moiety showed higher activity compared to those derivatives with phenylamino group (compared 4aa–4df with 4ea–4ef). The structure and position of substituents on the ring B and ring C had significant effects on the activity. As for ring B, the presence of ACH3 and AOCH3 electron-donating substituents slightly decreased the activity to A. alternate (compared 4aa with 4ba, compared 4am with 4ae). Different MIC values against the other

three fungal exhibited that the introduction of electron-donating substituents to ring B was less important for enhancement of the activity than substituents on ring C. When the ring B was substitute by pyridyl, 4dc and 4de showed higher activity than 4af and 4ae against A. alternate, and 4da-4df showed a lower activity than other substituents on ring B to P. capsici, C. gloeosporioides, V. mali. As for ring C, the presence of OH, 3-OCH3, 4-OH, 4-CH (CH3)2, 4-N(CH3)2, styryl, 4-CHO and iPr group all led to an increase of the sensitivity against P. capsici, C. gloeosporioides, V. mali and a

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J. Zhang et al. / Bioorg. Med. Chem. Lett. xxx (2016) xxx–xxx

Scheme 2. Possible mechanism for the formation of 3-acrylamide quinazolinones.

decrease of activity against A. alternate. It was worth noting that the introduction of hydroxy group and 3-OCH3, 4-OH substituent had strongly improved the activity against P. capsici. Besides, the introduction of 4-OCH3, 4-CHO, 3-pyridyl and styryl remarkably enhanced the activity against C. gloeosporioides. Similar cases were observed against V. mali for introduction of styryl or CH(CH3)2 to the 4-site on ring C. To further explore the potential mechanism of acylamino moiety and provide guidance for new scaffolds design, synthesized compounds 4ag, 4bb, 4bc with the significant vitro antifungal activity and broad antifungal spectrum and compounds 4ea with moderate antifungal activities were chosen for docking. Compounds 4ag, 4bb and 4bc all adopted the similar mode and location in the active site (Fig. 2(a)), whereas 4ea (green sticks in Fig. 2) laid in a different conformation in the active site. The lowest binding energy and inhibition constant of four compounds (4ag, 4bb, 4bc and 4ea) were listed in Table 3. Compounds 4bc achieved a lower binding energy and inhibition constant than others suggested a good agreement with the observations from the vitro antifungal results. It could be illustrated in Fig. 2(b) that the docking of compounds 4bc fit neatly into the binding site of chitinase. The binding details were emphasized in Fig. 2(c) that the hydrogen bond (O. . .H. . .N: 1.9 nm) was between the carbonyl oxygen of acylamino and the side chain Trp137, and quinazolinone moiety and ring B and C formed hydrophobic contact with amino acids Trp384, Asp385, Asp175, Tyr245, Asp246, Trp52. The critical interaction formed by compound 4bc with 2A3E (chitinase) was resembled two original ligands allosamizoline and N-acetyl-D-allosamine. When compounds filled into this site, the enzyme was not available for chitin to gain access to the active site and couldn’t degrade the substrates. Both the compound 4bc and original ligand allosamizoline form the same hydrogen bond to the Trp137, which was crucial for increasing the binding affinity and antifungal activity. Compared with the two original ligands, compound 4bc didn’t form any hydrogen bonds to Arg57, Glu322, Thr138, which played important roles in binding with allosamizoline and N-acetyl-D-allosamine. The side chain Asp385 formed part of the binding cavity of hydrophobic contact with compound 4bc, which was also different from the allosamizoline and N-acetyl-D-allosamine. It was inspiring to compare the binding affinities of compound 4bc with original ligands, and it would help designing more potent compounds with promising features. In conclusion, an efficient one-pot, three-component synthesis of quinazolinone derivatives containing 3-acrylamino motif was carried out using CeO2 nanoparticles as catalyst. And the antifungal activity of all compounds was evaluated against four plant pathogenic fungi in vitro. Among the thirty-nine synthesized compounds, seventeen compounds (4ak, 4am, 4ba–4bf, 4cb–4ce, 4da–4dd, 4df) were reported firstly. Furthermore, 4ag, 4bb, 4bc

Figure 2. Docking of 4ag, 4bb, 4bc and 4ea to the family 18 chitinase (2A3E): (a) overlay of docked conformations for compounds 4ag, 4bb, 4bc (depicted in grey) and 4ea (depicted in green); (b) Connolly surface of docking pose of 2A3E with compound 4bc shown as a stick model; (c) hydrogen bonds between the enzyme and compounds 4bc shown as red dashed lines and distances in Å units. Other residues were labeled to form a hydrophobic contact with ligand 4bc.

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J. Zhang et al. / Bioorg. Med. Chem. Lett. xxx (2016) xxx–xxx Table 3 Docking results of the synthesized compounds 4ag, 4bb, 4bc and 4ea Entry

Ligand

1 2 3 4

4ag 4bb 4bc 4ea

Lowest binding energy (kcal/mol) 9.41 9.02 9.94 8.40

Inhibition constant (molar) 1.26  10 2.43  10 5.18  10 6.93  10

6 6 7 6

showed significant activity and broad antifungal spectrum as the commercial fungicide ketoconazole. The structure–activity relationships showed that the importance of the amid moiety and the different substituents on ring B and C have variable effects on activities. A probably mechanism was supposed by molecular docking that the hydrogen bonds to the Trp137 and the hydrophobic contact to Trp384, Trp52, Thr138 and Asp385 played an important roles when binding with the protein. Thus the present results were useful and meaningful for the design, synthesis and development of novel quinazolinone antifungal agents and the further modification of the structure. Acknowledgments The work was supported by Scientific Research Project Item for Key Laboratory of Shaanxi Province Education Department, China (No. 2010JS056), Natural Science Basic Research Plan in Shaanxi Province of China (No. 2014JQ2064), and the Foundation for Young Scholars of Shaanxi University of Science & Technology (No. BJ1226). Training Programs of Innovation and Entrepreneurship for Undergraduates of Shaanxi Province (No. 1219). Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.bmcl.2016.03. 052. References and notes 1. Gonzalez-Fernandez, R.; Jorrin-Novo, J. V. J. Proteome. Res. 2012, 11, 3. 2. Savary, S.; Teng, P. S.; Willocquet, L.; Forrest, W.; Nutter, J. Annu. Rev. Phytopathol. 2006, 44, 89. 3. Atanda, S. A.; Pessu, P. O.; Agoda, S.; Isong, I. U.; Adekalu, O. A.; Echendu, M. A.; Falade, T. C. Afr. J. Microbiol. Res. 2011, 5, 4373. 4. Azevedo, M.-M.; Faria-Ramos, I.; Cruz, L. C.; Pina-Vaz, C.; Gonçalves Rodrigues, A. J. Agric. Food Chem. 2015, 63, 7463.

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