Pitsubcosides A-L, highly esterified eudesmane sesquiterpenoid glycosides with antibacterial activity from Pittosporum subulisepalum and their mechanism.
Pittosporum subulisepalum
antibacterial activity
esterified glycosides
pitsubcosides
sesquiterpenoid
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
revised:
29
04
2023
received:
06
04
2023
accepted:
02
05
2023
medline:
4
9
2023
pubmed:
4
5
2023
entrez:
4
5
2023
Statut:
ppublish
Résumé
Plants from the genus Pittosporum are traditionally used as antibacterial, antifungal and antiviral agents. A bioassay evaluation of the extract of Pittosporum subulisepalum revealed antibacterial activity. This study focused on the discovery of the antibacterial metabolism in P. subulisepalum, as well as the modes of action of its active components. A chemical investigation of an ethyl acetate (EtOAc) extract of the aerial parts of P. subulisepalum led to the isolation of 12 previously undescribed eudesmane sesquiterpenoid glycoside esters (ESGEs), pitsubcosides A-L (1-12). Their structures were elucidated by extensive spectroscopic analysis, including one- and two-dimensional NMR, high-resolution electrospray ionization mass spectrometry, electronic circular dichroism spectra and single-crystal X-ray crystallography analysis or by comparing with authentic samples. The new ESGEs were characterized by their highly esterified glycoside moieties. Among them, compounds 1-3, 5 and 8 showed a moderate inhibitory effect against Staphylococcus aureus, methicillin-resistant S. aureus (MRSA), Bacillus cereus, Bacillus subtilis, Pseudomonas syringae pv. actinidiae (Psa) and Erwinia carotovora with minimum inhibitory concentrations (MICs) ranging from 3.13 to 100 μm. Among them, compounds 3 and 5 showed remarkable antibacterial activity against S. aureus and Psa with MIC values of 6.25 and 3.13 μm, respectively. Live bacterial mass and the biofilms of S. aureus and Psa were quantified using methyl tetrazolium and crystal violet assays. Fluorescence microscopy and scanning electron microscopy experiments revealed an antibacterial mechanism of cell membrane architectural disruption. The results suggest that ESGEs possess great potential for the development of antibacterial agents to control plant pathogens. © 2023 Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
Plants from the genus Pittosporum are traditionally used as antibacterial, antifungal and antiviral agents. A bioassay evaluation of the extract of Pittosporum subulisepalum revealed antibacterial activity. This study focused on the discovery of the antibacterial metabolism in P. subulisepalum, as well as the modes of action of its active components.
RESULTS
RESULTS
A chemical investigation of an ethyl acetate (EtOAc) extract of the aerial parts of P. subulisepalum led to the isolation of 12 previously undescribed eudesmane sesquiterpenoid glycoside esters (ESGEs), pitsubcosides A-L (1-12). Their structures were elucidated by extensive spectroscopic analysis, including one- and two-dimensional NMR, high-resolution electrospray ionization mass spectrometry, electronic circular dichroism spectra and single-crystal X-ray crystallography analysis or by comparing with authentic samples. The new ESGEs were characterized by their highly esterified glycoside moieties. Among them, compounds 1-3, 5 and 8 showed a moderate inhibitory effect against Staphylococcus aureus, methicillin-resistant S. aureus (MRSA), Bacillus cereus, Bacillus subtilis, Pseudomonas syringae pv. actinidiae (Psa) and Erwinia carotovora with minimum inhibitory concentrations (MICs) ranging from 3.13 to 100 μm. Among them, compounds 3 and 5 showed remarkable antibacterial activity against S. aureus and Psa with MIC values of 6.25 and 3.13 μm, respectively. Live bacterial mass and the biofilms of S. aureus and Psa were quantified using methyl tetrazolium and crystal violet assays. Fluorescence microscopy and scanning electron microscopy experiments revealed an antibacterial mechanism of cell membrane architectural disruption.
CONCLUSION
CONCLUSIONS
The results suggest that ESGEs possess great potential for the development of antibacterial agents to control plant pathogens. © 2023 Society of Chemical Industry.
Substances chimiques
Glycosides
0
Plant Extracts
0
Anti-Bacterial Agents
0
Cardiac Glycosides
0
Sesquiterpenes
0
Sesquiterpenes, Eudesmane
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3471-3485Subventions
Organisme : shaanxi agricultural special fund projects
Organisme : the Undergraduate Innovation Fund of Northwest A&F University, China
Informations de copyright
© 2023 Society of Chemical Industry.
Références
Atkinson D, Litterick AM, Walker KC, Walker R and Watson CA, Crop protection-what will shape the future picture? Pest Manage Sci 60:105-112 (2004).
Huang ZD, Tang W, Jiang TS, Xu XT, Kong K, Shi SP et al., Structural characterization, derivatization and antibacterial activity of secondary metabolites produced by termite-associated BYF17. Pest Manage Sci 79:1800-1808 (2023).
Liu DY, Zhang J, Zhao L, He WJ, Liu ZJ, Gan XH et al., First discovery of novel pyrido[1,2-a]pyrimidinone mesoionic compounds as antibacterial agents. J Agric Food Chem 67:11860-11866 (2019).
Cantrell CL, Dayan FE and Duke SO, Natural products as sources for new pesticides. J Nat Prod 75:1231-1242 (2012).
El Dib RA, Eskander J, Mohamed MA and Mohammed NM, Two new triterpenoid estersaponins and biological activities of Pittosporum tobira 'Variegata' (Thunb.) W. T. Aiton leaves. Fitoterapia 106:272-279 (2015).
Jugreet BS, Lall N, Lambrechts IA, Reid A, Maphutha J, Nel M et al., In vitro and in silico pharmacological and cosmeceutical potential of ten essential oils from aromatic medicinal plants from the Mascarene Islands. Molecules 27:8705-8720 (2022).
Ramanandraibe V, Rakotovao M, Andriamaharavo RN, Bessiere JM, Ravaonindrina N and Ramanoelina ARP, Composition and antimicrobial activity of the leaf and fruit essential oil of Pittosporum viridiflorum Culofondis var. Viridiflorum. J Essent Oil Res 12:650-652 (2000).
Medeiros JR, Campos LB, Nendonca SC, Davin LB and Lewis NG, Composition and antimicrobial activity of the essential oils from invasive species of the Azores, Hedychium gardnerianum and Pittosporum undulatum. Phytochemistry 64:561-565 (2003).
John AJ, Karunakaran VP, George V, Pradeep NS and Sethuraman MG, Constituents and antibacterial activity of the essential oils from the leaves and fruits of Pittosporum viridulum. J Essent Oil Res 19:591-593 (2007).
Guadalupe TB, Salvador OS, Griselda GG, Agustin HJ, Sandra GMR and Julio CCH, The resistance of seven host plants to Tetranychus merganser boudreaux (Acari: Tetranychidae). Insects 13:167-177 (2022).
Mendes SAC, Mansoor TA, Rodrigues A, Armas JB and Ferreira MU, Anti-inflammatory guaiane-type sesquiterpenes from the fruits of Pittosporum undulatum. Phytochemistry 95:308-314 (2013).
Wandji BA, Bomba FDT, Nkeng-Efouet PA, Piegang BN, Kamanyi A and Nguelefack TB, Anti-hyperalgesic activity of the aqueous and methanol extracts of the leaves of Pittosporum mannii Hook on CFA-induced persistent inflammatory pain. Inflammopharmacology 26:197-205 (2018).
Zhao HX, Nie TT, Guo HJ, Li J and Bai H, Two new neolignan glycosides from Pittosporu glabratum Lindl. Phytochem Lett 5:240-243 (2012).
Wandji BA, Bomba FCT, Awouafack MD and Nkeng-Efouet PA, Antinociceptive effects of the aqueous and methanol extracts of the leaves of Pittosporum mannii Hook. F (Pittosporaceae) in mice. J Ethnopharmacol 187:224-231 (2016).
Joseph N, Esther NLT, Benoit NT, Desire DDP, Bibi-Farouck AO, Theophile D et al., Effect of the aqueous extract of Pittosporum mannii Hook. F. (Pittosporaceae) stem barks on spontaneous and spasmogen-induced contractile activity of isolated rat duodenum. J Ethnopharmacol 172:1-9 (2015).
Takaoka D, Kawahara H, Ochi S, Hiroi M, Nozaki H, Nakayama M et al., The structures of sesquiterpene glycosides from Pittosporum tobira Ait. Chem Lett 15:1121-1124 (1986).
Suga T, Munesada K, Ogihara K, Morita T and Shirai T, The structure of a new sesquiterpene glycoside from the flowers of Pittosporum tobira. Chem Lett 27:445-448 (1988).
Wu X, Li Y, Zhang M, Shi YJ, Li ZM, Liu Y et al., A new sesquiterpene glycoside from Pittosporum kerrii. Chem Nat Compd 54:1091-1093 (2018).
Mendes S, Madruga J, Lima E and Ferreira MJU, Phytochemical study of Pittosporum undulatum: searching for new guaiane-type sesquiterpenes with anti-inflammatory acitvity. Planta Med 80:1428-1430 (2014).
Eparvier V, Thoison O, Bousserouel H, Gueritte F, Sevenet T and Litaudon M, Cytotoxic farnesyl glycosides from Pittosporum pancher. Phytochemistry 68:604-608 (2007).
Carrillo MR, Mitaine-Offer AC, Miyamoto T, Tanaka C, Pouysegu L, Quideau S et al., Oleanane-type glycosides from Pittosporum tenuifolium “variegatum” and P. tenuifolium “gold star”. Phytochemistry 140:166-173 (2017).
Backer C, Jenett-Siems K, Siems K, Wurster M, Bodtke A, Chamseddin C et al., Triterpene glycosides from the leaves of Pittosporum angustifolium. Planta Med 79:1461-1469 (2013).
Seo Y, Berger JM, Hoch J, Neddermann KM, Bursuker I, Mamber SW et al., A new triterpen saponin from Pittosporum viridiflorum from the Madagascar rainforest. J Nat Prod 65:65-68 (2002).
Feng C, Li BG, Gao XP, Qi HY and Zhang GL, A new triterpene and an antiarrhythmic liriodendrin from Pittosporum brevicalyx. Arch Pharm Res 33:1927-1932 (2010).
Moon HI and Park WH, Four carotenoids from Pittosporum tobira protect primary cultured rat cortical cells from glutamate-induced toxicity. Phytother Res 24:625-628 (2010).
Maoka T, Akimoto N, Kuroda Y, Hashimoto K and Fujiwara Y, Pittosporumxanthins, cycloaddition products of carotenoids with α-tocopherol from seeds of Pittosporum tobira. J Nat Prod 71:622-627 (2008).
Maoka T, Fujiwara Y, Hashimoto K and Akimoto N, 5-Hydroxy-seco-carotenoids from Pittosporum tobira. Phytochemistry 67:2120-2125 (2006).
Fujiwara Y, Maruwaka H, Toki F, Hashimoto K and Maoka T, Structure of three new carotenoids with a 3-methoxy-5-keto-5,6-seco-4,6-cyclo-β end group from the seeds of Pittosporum tobira. Chem Pharm Bull 49:985-987 (2001).
Fujiwara Y and Maoka T, Structure of pittosporumxanthins A1 an A2, novel C69 carotenoids from the seeds of Pittosporum tobira. Tetrahedron Lett 42:2693-2696 (2001).
Fujiwara Y, Hashimoto K, Manabe K and Maoka T, Structures of tobiraxanthins A1, A2, A3, B, C and D, new carotenoids from the seeds of Pittosporum tobira. Tetrahedron Lett 43:4385-4388 (2002).
Chou TH, Chen IS, Hwang TL, Wang TC, Lee TH, Cheng LY et al., Phthalides from Pittosporum illicioides var. illicioides with inhibitory activity on superoxide generation and elastase release by neutrophils. J Nat Prod 71:1692-1695 (2008).
Xiao BK, Yang JY, Liu YR, Dong JX and Huang RQ, A new phthalide from Pittosporum illicioides. Chem Nat Compd 51:634-636 (2015).
Ragasa CY, Rideout JA, Tierra DS and Coll JC, Sesquiterpene glycosides from Pittosporum pentandrum. Phytochemistry 45:545-547 (1997).
Jakupovic J, Grenz M, Bohlmann F, Rustaiyan A and Koussari S, Sesquiterpene glycosides from Calendula persica. Planta Med 54:254-256 (1988).
Zhang XY, Liu Y, Deng JL, Xia JK, Zhang Q, Chen X et al., Structurally diverse sesquiterpenoid glycoside esters from Pittosporum qinlingense with anti-neuroinflammatory activity. J Nat Prod 85:115-126 (2022).
Martinez M, Flores G and De Vivar AR, Guayulins C and D from guayule (Parthenium argentatum). J Nat Prod 49:1102-1103 (1986).
De Tommasi N and Pizza C, Structure and in vitro antiviral activity of sesquiterpene glycosides from Calendula arvensis. J Nat Prod 53:830-835 (1990).
Zhang T, Gong T, Yang Y, Chen RY and Yu DQ, Two new eudesmanolides from Inula racemosa and their bioactivities. Phytochem Lett 5:229-232 (2012).
Zan K, Chen XQ, Chai XY, Wu Q, Fu Q, Zhou SX et al., Two new cytotoxic eudesmane sesquiterpenoids from Artemisia anomala. Phytochem Lett 5:313-315 (2012).
Tsai CJ, Liang JW and Lin HR, Sesquiterpenoids from Atractylodes macrocephala act as farnesoid X receptor and progesterone receptor modulators. Bioorg Med Chem Lett 22:2326-2329 (2012).
Sha BT, Huang R, Zhang QG, Guan SN, Ding JQ, Liu XZ et al., Four anti-inflammatory aromadendrane sesquiterpenoid fucosides and other constituents from Pittosporum glabratum var. neriifolium. Phytochem Lett 55:17-21 (2023).
Deng JL, Zhang QG HR, Sha BT, Wang MC, Deng SY et al., Further sesquiterpenoids from Pittosporum qinlingense and their anti-inflammatory activity. Fitoterapia 162:105292-105298 (2022).
Delectis Florae Reipublicae Popuparis Sinicae Abendae Academiae Sinicae Edita., Flora Republicae Popularis Sinicae (Flora of China), Vol. 35. Science Press, Beijing, p. 8 (1979).
Conflex 6.7. Conflex Corp, Tokyo Yokohama, Japan (2010).
Yan DW, Huang CD, Zheng HH, Zhao N, Feng XL, Ma SJ et al., Meroterpene-like α-glucosidase inhibitors based on biomimetic reactions starting from β-caryophyllene. Molecules 25:260-275 (2020).
Ma SJ, Yu J, Yan DW, Wang DC, Gao JM and Zhang Q, Meroterpene-like compounds derived from β-caryophyllene as potent α-glucosidase inhibitors. Org Biomol Chem 16:9454-9460 (2018).
Lin LB, Xiao J, Zhang Q, Han R, Xu B, Yang SX et al., Eremophilane sesquiterpenoids with antibacterial and anti-inflammatory activities from the endophytic fungus Septoria rudbeckiae. J Agric Food Chem 69:11878-11889 (2021).
Zhang XY, Wang LK, Mu HB, Wang DD and Yu YB, Synergistic antibacterial effects of Buddleja albiflora metabolites with antibiotics against Listeria monocytogenes. Lett Appl Microbiol 68:38-47 (2019).
Djordjevic D, Wiedmann M and McLandsborough M, Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68:2950-2958 (2002).
Schillaci D, Arizza V, Dayton T, Camarda L and Stefano VD, In vitro antibiofilm activity of Boswellia spp. oleogum resin essential oils. Lett Appl Microbiol 47:433-438 (2008).
Ding L and Hertweck C, Oxygenated geosmins and plant-like eudesmanes from a bacterial mangrove endophyte. J Nat Prod 83:2207-2211 (2020).
Adinarayana D and Syamasundar KV, A new sesquiterpene alcohol from Pterocarpus marsupium. Phytochemistry 21:1083-1085 (1982).
El-Askary HI, Meselhy MR and Galal AM, Sesquiterpenes from Cymbopogon proximus. Molecules 8:670-677 (2003).
Zhao Y, Yue JM, He YN, Lin ZW and Sun HD, Eleven new eudesmane derivatives from Laggera pterodonta. J Nat Prod 60:545-549 (1997).
D'Ambrosio M, Ciocarlan A, Colombo E, Guerriero A, Pizza C, Sangiovanni E et al., Structure and cytotoxic activity of sesquiterpene glycoside esters from Calendula officinalis L.: studies on the conformation of viridiflorol. Phytochemistry 117:1-9 (2015).
Yang JL, Liu LL and Shi YP, Two new eudesmane sesquiterpoids from the flowers of Chrysanthemum indicum. Nat Prod Bioprospect 9:145-148 (2019).
Katsutani K, Sugimoto S, Yamano Y, Otsuka H, Matsunami K and Mizuta T, Eudesmane-type sesquiterpene glycosides: sonneratiosides A-E and eudesmol β-D-glucopyranoside from the leaves of Sonneratia alba. J Nat Med 74:119-126 (2020).
Evans FE, Miller DW, Cairns T, Baddeley GV and Wenkert E, Structure analysis of proximadiol (cryptomeridiol) by 13C NMR spectroscopy. Phytochemistry 21:937-938 (1982).
Ragasa CY, Kristin AL and Rideout JA, Antifungal metabolites from Blumea balsamifera. Nat Prod Res 19:231-237 (2005).
Yan YH, Zhang LX, Liu X, Zhu Q, Wang Y, Liang HY et al., Phytochemical and chemotaxonomic study of Pulsatilla cernua (Thunb.) Bercht Ex J Presl. Biochem Syst Ecol 97:104291-104294 (2021).
Ogihara K, Munesada K and Suga T, Sesquiterpene glycosides and other terpene constituents from the flowers of Pittosporum tobira. Phytochemistry 28:3085-3091 (1989).