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Exploring new applications of tulip tree (Liriodendron tulipifera L.): leaf essential oil as apoptotic agent for human glioblastoma

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Abstract

Liriodendron tulipifera L. (Magnoliaceae), also known as “tulip tree,” is a hardwood plant native to North America, cultivated all over the world and used on an industrial level, especially for its fine wood and to make honey. It has also been traditionally exploited for its antimalarial properties. However, our knowledge about the bioactivity of its essential oil remains patchy. In this research, we focused on the biological evaluation of the volatile fractions obtained from different parts of the plant which are normally discharged by industry, including leaves, flowers, and fruits. For the purpose, the essential oils were obtained by hydrodistillation and analyzed by gas chromatography-mass spectrometry (GC-MS). Then, they were evaluated as radical scavenging, antioxidant, antimicrobial, and antiproliferative agents by using DPPH, ABTS, FRAP, disk diffusion, and MTT methods, respectively. The significant toxicity exhibited on human tumor cells, namely A375 malignant melanoma, HCT116 colon carcinoma, MDA-MB 231 breast adenocarcinoma, and T98G glioblastoma multiforme cell lines, prompted us to study the mechanism of action by acridine orange/ethidium bromide double staining and caspase 3 assays. Our findings shed light on the potential applications of tulip tree derivatives as anticancer drugs.

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References

  • Adams R (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Publishing Corp, Carol Stream

    Google Scholar 

  • Afshar FH, Maggi F, Iannarelli R, Cianfaglione K, Isman MB (2017) Comparative toxicity of Helosciadium nodiflorum essential oils and combinations of their main constituents against the cabbage looper, Trichoplusia ni (Lepidoptera). Ind Crops Prod 98:46–52

    Article  CAS  Google Scholar 

  • Amorati R, Foti MC, Valgimigli L (2013) Antioxidant activity of essential oils. J Agric Food Chem 61:10835–10847

    Article  CAS  Google Scholar 

  • Arévalo ÁST, Erices JI, Uribe DA, Howden J, Niechi I, Muñoz S, Martín RS, Monrás CAQ (2017) Current therapeutic alternatives and new perspectives in glioblastoma multiforme. Curr Med Chem 24:2781–2795

    Article  CAS  Google Scholar 

  • Arnao MB (2000) Some methodological problems in the determination of antioxidant activity using chromogen radicals: a practical case. Trends Food Sci Technol 11:419–421

    Article  CAS  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils - a review. Food Chem Toxicol 46:446–475

    Article  CAS  Google Scholar 

  • Banumathi B, Vaseeharan B, Periyannan R, Prabhu NM, Ramasamy P, Murugan K, Canale A, Benelli G (2017) Exploitation of chemical, herbal and nanoformulated acaricides to control the cattle tick, Rhipicephalus (Boophilus) microplus – A review. Vet Parasitol 244:102–110

    Article  CAS  Google Scholar 

  • Benelli G (2018) Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology. Environ Sci Pollut Res 25:10149–10150

    Article  Google Scholar 

  • Benelli G, Pavela R (2018a) Repellence of essential oils and selected compounds against ticks – a systematic review. Acta Trop 179:47–54

    Article  CAS  Google Scholar 

  • Benelli G, Pavela R (2018b) Beyond mosquitoes – essential oil toxicity and repellency against bloodsucking insects. Ind Crops Prod 117:382–392

    Article  CAS  Google Scholar 

  • Benelli G, Pavela R, Ricciutelli M, Lupidi G, Maggi F (2017) Efficacy of the volatile oil from water celery (Helosciadium nodiflorum, Apiaceae) against the filariasis vector Culex quinquefasciatus, the housefly Musca domestica and the African cotton leafworm Spodoptera littoralis. Chem Biodivers 14:e1700376

    Article  CAS  Google Scholar 

  • Benelli G, Pavela R, Petrelli R, Cappellacci L, Canale A, Senthil-Nathan S, Maggi F (2018a) Not just popular spices! Essential oils from Cuminum cyminum and Pimpinella anisum are toxic to insect pests and vectors without affecting non-target invertebrates. Ind Crops Prod 124:236–243

    Article  CAS  Google Scholar 

  • Benelli G, Pavela R, Petrelli R, Cappellacci L, Santini G, Fiorini D, Sut S, Dall’Acqua S, Canale A, Maggi F (2018b) The essential oil from industrial hemp (Cannabis sativa L.) by-products as an effective tool for insect pest management in organic crops. Ind Crops Prod 122:308–315

    Article  CAS  Google Scholar 

  • Boik J (2001) Natural compounds in cancer therapy. Oregon Medical Press, LLC, Minnesota

    Google Scholar 

  • Brunetti A, Marinelli O, Morelli MB, Iannarelli R, Amantini C, Russotti D, Santoni G, Maggi F, Nabissi M (2019) Isofuranodiene synergizes with temozolomide in inducing glioma cells death. Phytomedicine 52:51–59

    Article  CAS  Google Scholar 

  • Byrne CE, Nagle DC (1997) Carbonization of wood for advanced materials applications. Carbon 35:259–266

    Article  CAS  Google Scholar 

  • Casiglia S, Bruno M, Bramucci M, Quassinti L, Lupidi G, Fiorini D, Maggi F (2017) Kundmannia sicula (L.) DC: a rich source of germacrene D. J Essent Oil Res 29:437–442

    Article  CAS  Google Scholar 

  • Chellappandian M, Thanigaivel A, Vasantha-Srinivasan P, Edwin ES, Ponsankar A, Selin-Rani S, Kalaivani K, Senthil-Nathan S, Benelli G (2018) Toxicological effect of Sphaeranthus indicus Linn. (Asteraceae) leaf essential oil against human disease vectors Culex quinquefasciatus Say, Aedes aegypti Lin. and their impact on beneficial mosquito predator. Environ Sci Poll Res 25:10294–10306

    Article  CAS  Google Scholar 

  • Chiu CC, Chou HL, Wu PF, Chen HL, Wang HM, Chen CY (2012) Bio-functional constituents from the stems of Liriodendron tulipifera. Molecules 17:4357–4372

    Article  CAS  Google Scholar 

  • Clinical and Laboratory Standards Institute (CLSI) (2011) Performance standards for antimicrobial susceptibility testing, 21th informational supplement (M100–S21). CLSI, Wayne

    Google Scholar 

  • Cotter TG, Martin SG (1996) Techniques in Apoptosis. A Use’s Guide. Portland Press Ltd, London, pp 7–9

    Google Scholar 

  • Curvelo JAR, Marques AM, Barreto ALS, Romanos MTV, Portela MB, Kaplan MAC, Soares RMA (2014) A novel nerolidol-rich essential oil from Piper claussenianum modulates Candida albicans biofilm. J Med Microbiol 63:697–702

    Article  CAS  Google Scholar 

  • Dall’Acqua S, Peron G, Ferrari S, Gandin V, Bramucci M, Quassinti L, Martonfi P, Maggi F (2017) Phytochemical investigations and antiproliferative secondary metabolites from Thymus alternans growing in Slovakia. Pharm Biol 55:1162–1170

    Article  CAS  Google Scholar 

  • Dudai N, Poljakoff-Mayber A, Mayer AM, Putievsky E, Lerner HR (1999) Essential oils as allelochemicals and their potential use as bioherbicides. J Chem Ecol 25:1079–1089

    Article  CAS  Google Scholar 

  • FFNSC2 (2012) Flavors and fragrances of natural and synthetic compounds. Mass Spectral Database. Shimadzu Corps, Kyoto

    Google Scholar 

  • Fiorini D, Molle A, Nabissi M, Santini G, Benelli G, Maggi F (2019) Valorizing industrial hemp (Cannabis sativa L.) by-products: cannabidiol enrichment in the inflorescence essential oil optimizing sample pre-treatment prior to distillation. Ind Crops Prod 128:581–589

    Article  CAS  Google Scholar 

  • Fonseca DV, Salgado PRR, de Carvalho FL, Salvadori MGSS, Penha ARS, Leite FC, Borges CJS, Piuvezam MR, de Morais Pordeus LC, Sousa DP, Almeida RN (2016) Nerolidol exhibits antinoceptive and anti-inflammatory activity: involvement of the GABAergic system and proinflammatory cytokines. Fund Clin Pharmacol 30:14–22

    Article  CAS  Google Scholar 

  • Graziose R, Rathinasabapathy T, Lategan C, Poulev A, Smith PJ, Grace M, Lila MA, Raskin I (2011) Antiplasmodial activity of aporphine alkaloids and sesquiterpene lactones from Liriodendron tulipifera L. J Ethnopharmacol 133:26–30

    Article  CAS  Google Scholar 

  • Hsu CYH, Chen CL (1991) Antimicrobial activities of aporphine alkaloids isolated from heartwood and discolored sapwood of Liriodendron tulipifera. Holzforschung 45:325–332

    Article  CAS  Google Scholar 

  • Iannarelli R, Marinelli O, Morelli MB, Santoni G, Amantini C, Nabissi M, Maggi F (2018) Aniseed (Pimpinella anisum L.) essential oil reduces pro-inflammatory cytokines and stimulates mucus secretion in primary airway bronchial and tracheal epithelial cell lines. Ind Crops Prod 114:81–86

    Article  CAS  Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  CAS  Google Scholar 

  • Kang YF, Liu CM, Kao CL, Chen CY (2014) Antioxidant and anticancer constituents from the leaves of Liriodendron tulipifera. Molecules 19:4234–4245

    Article  CAS  Google Scholar 

  • Kang ZW, Liu FH, Zhang ZF, Tian HG, Liu TX (2018) Volatile β-ocimene can regulate developmental performance of peach aphid Myzus persicae through activation of defense responses in Chinese cabbage Brassica pekinensis. Front Plant Sci 9:708

    Article  Google Scholar 

  • Kaur G, Verma N (2015) Nature curing cancer—review on structural modification studies with natural active compounds having anti-tumor efficiency. Biotechnol Rep 6:64–78

    Article  Google Scholar 

  • Keeler HL (1902) Our Native Trees and how to identify them; a popular study of their habits and their peculiarities. Scribner, New York

    Book  Google Scholar 

  • Lee K, Lee JH, Kim SI, Cho MH, Lee J (2014) Anti-biofilm, anti-hemolysis, and anti-virulence activities of black pepper, cananga, myrrh oils, and nerolidol against Staphylococcus aureus. Appl Microbiol Biotechnol 98:9447–9457

    Article  CAS  Google Scholar 

  • Li X, Wang G, Zhao J, Ding H, Cunningham C, Chen F, Flynn DC, Reed E, Li QQ (2005) Antiproliferative effect of β-elemene in chemoresistant ovarian carcinoma cells is mediated through arrest of the cell cycle at the G2-M phase. Cell Mol Life Sci 62:894–904

    Article  CAS  Google Scholar 

  • Li QQ, Wang G, Huang F, Li JM, Cuff CF, Reed E (2013a) Sensitization of lung cancer cells to cisplatin by β-elemene is mediated through blockade of cell cycle progression: antitumor efficacies of β-elemene and its synthetic analogs. Med Oncol 30:488

    Article  CAS  Google Scholar 

  • Li WJ, Lin YC, Wu PF, Li WW, Lin Y, Wu PF, Wen ZH, Liu PL, Chen CY, Wang HM, Liu PL, Chen CY, Wang HM (2013b) Biofunctional constituents from Liriodendron tulipifera with antioxidants and anti-melanogenic properties. Int J Mol Sci 14:1698–1712

    Article  CAS  Google Scholar 

  • Liu K, Liu PC, Liu R, Wu X (2015) Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med Sci Monit Basic Res 21:15–20

    Article  Google Scholar 

  • Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol 131:803–820

    Article  Google Scholar 

  • Maggi F, Giuliani C, Fico G, Ricciutelli M, Bramucci M, Quassinti L, Petrelli D, Vitali LA, Cianfaglione K, Tirillini B, Sut S, Dall’Acqua S (2019) Secondary metabolites, secretory structures and biological activity of water celery (Apium nodiflorum (L.) Lag.) growing in central Italy. Plant Biosyst 153:325–335

    Article  Google Scholar 

  • Miller SL, Villanueva HE, Palazzo MC, Wright BS, Setzer WN (2009) Seasonal variation and bioactivity in the leaf oil of Liriodendron tulipifera growing in Huntsville, Alabama. Nat Prod Comm 4:839–843

    CAS  Google Scholar 

  • Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant–herbivore chemical interactions. Trends Plant Sci 19:29–35

    Article  CAS  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  Google Scholar 

  • Mustafa AM, Eldahmy SI, Caprioli G, Bramucci M, Quassinti L, Lupidi G, Beghelli D, Vittori S, Maggi F (2018) Chemical composition and biological activities of the essential oil from Pulicaria undulata (L.) C. A. Mey. Growing wild in Egypt. Nat Prod Res 4:1–5

    Article  CAS  Google Scholar 

  • Nabavi SM, Nabavi SF, Sureda A, Caprioli G, Iannarelli R, Sokeng AJT, Braidy N, Khanjani S, Moghaddam AH, Atanasov AG, Daglia M, Maggi F (2018) The water extract of tutsan (Hypericum androsaemum L.) red berries exerts antidepressive-like effects and in vivo antioxidant activity in a mouse model of post-stroke depression. Biomed Pharmacother 99:290–298

    Article  CAS  Google Scholar 

  • Ngahang Kamte SL, Ranjbarian F, Cianfaglione K, Sut S, Dall’Acqua S, Bruno M, Afshar FH, Iannarelli R, Benelli G, Cappellacci C, Hofer A, Maggi F, Petrelli R (2018) Identification of highly effective antitrypanosomal compounds in essential oils from the Apiaceae family. Ecotoxicol Environ Saf 156:154–165

    Article  CAS  Google Scholar 

  • Ngo TC, Dao DQ, Nguyen MT, Nam PC (2017) A DFT analysis on the radical scavenging activity of oxygenated terpenoids present in the extract of the buds of Cleistocalyx operculatus. RSC Advances 7:39686–39698

  • Nishii Y, Watanabe K, Yoshida T, Okayama T, Takahashi S, Tanabe Y (1997) Total synthesis of (−)-periplanones C and D. Their pheromonal activities against three Periplaneta species. Tetrahedron 53:7209–7218

    Article  CAS  Google Scholar 

  • NIST17 (2017) Mass Spectral Library (NIST/EPA/NIH). National Institute of Standards and Technology, Gaithersburg

    Google Scholar 

  • Nogueira Neto JD, De Almeida AAC, Da Silva OJ, Dos Santos PS, De Sousa DP, De Freitas RM (2013) Antioxidant effects of nerolidol in mice hippocampus after open field test. Neurochem Res 38:1861–1870

    Article  CAS  Google Scholar 

  • Ornano L, Venditti A, Ballero M, Sanna C, Quassinti L, Bramucci M, Lupidi G, Papa F, Vittori S, Maggi F, Bianco A (2013) Chemopreventive and antioxidant activity of the chamazulene-rich essential oil obtained from Artemisia arborescens L. growing on the Isle of La Maddalena, Sardinia, Italy. Chem Biodivers 8:1464–1474

    Article  CAS  Google Scholar 

  • Pavela R, Benelli G (2016) Essential oils as eco-friendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007

    Article  CAS  Google Scholar 

  • Pavela R, Maggi F, Iannarelli R, Benelli G (2019) Plant extracts for developing mosquito larvicides: From laboratory to the field, with insights on the modes of action. Acta Trop 193:236–271

    Article  CAS  Google Scholar 

  • Petrelli R, Ranjbarian F, Dall’Acqua S, Papa F, Iannarelli R, Ngahang Kamte SL, Vittori S, Benelli G, Maggi F, Hofer A, Cappellacci L (2017) An overlooked horticultural crop, Smyrnium olusatrum, as a potential source of compounds effective against African trypanosomiasis. Parasitol Int 66:146–151

    Article  Google Scholar 

  • Pickett CH, Ball JC, Casanave KC, Klonsky KM, Jetter KM, Bezark LG, Schoenig SE (1996) Establishment of the ash whitefly parasitoid Encarsia inaron (Walker) and its economic benefit to ornamental street trees in California. Biol Control 6:260–272

    Article  Google Scholar 

  • Pignatti S (1982) Flora d’Italia, vol 1. Edagricole, Bologna, p 352

    Google Scholar 

  • Porter AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6:99–104

    Article  CAS  Google Scholar 

  • Quassinti L, Bramucci M, Lupidi G, Barboni L, Ricciutelli M, Sagratini G, Papa F, Caprioli G, Petrelli D, Vitali LA, Vittori S, Maggi F (2013) In vitro biological activity of essential oils and isolated furanosesquiterpenes from the neglected vegetable Smyrnium olusatrum L. (Apiaceae). Food Chem 138:808–813

    Article  CAS  Google Scholar 

  • Quassinti L, Maggi F, Barboni L, Ricciutelli M, Cortese M, Papa F, Garulli C, Kalogris C, Vittori S, Bramucci M (2014) Wild celery (Smyrnium olusatrum L.) oil and isofuranodiene induce apoptosis in human colon carcinoma cells. Fitoterapia 97:133–141

    Article  CAS  Google Scholar 

  • Ribble D, Goldstein NB, Norris DA, Shellman YG (2005) A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 5:12

    Article  CAS  Google Scholar 

  • Şahin F, Güllüce M, Daferera D, Sökmen A, Sökmen M, Polissiou M, Agar G, Özer H (2004) Biological activities of the essential oils and methanol extract of Origanum vulgare ssp. vulgare in the Eastern Anatolia region of Turkey. Food Control 15:549–557

    Article  CAS  Google Scholar 

  • Setzer WN, Schmidt JM, Noletto JA, Vogler B (2006) Leaf oil compositions and bioactivities of abaco bush medicines. Pharmacologyonline 3:794–802

    Google Scholar 

  • Smith AL, Campbell CL, Walker DB, Hanover JW, Miller RO (1988) Geographic variation in the essential oil monoterpenes of Liriodendron tulipifera L. Biochem Syst Ecol 16:627–630

    Article  CAS  Google Scholar 

  • Spencer CF, Koniuszy FR, Rogers EF, Shavel J, Easton NR, Kaczka EA, Kuehl FA, Phillips RF, Walti A, Folkers K, Malanga C, Seeler AO (1947) Survey of plants for antimalarial activity. Lloydia 10:145–174

    Google Scholar 

  • Thacher J (1967) American medical biography; or, memoirs of eminent physicians who have flourished in America, to which is prefixed a succinct history of medical science in the United States from the First Settlement of the Country. Milford House, New York

    Google Scholar 

  • Viuda-Martos M, Ruiz-Navajas Y, Sanchez-Zapata E, Fernández-López J, Pérez-Alvarez JA (2010) Antioxidant activity of essential oils of five spice plants widely used in a Mediterranean diet. Flavour Fragr J 25:13–19

    Article  CAS  Google Scholar 

  • Woguem V, Fogang HP, Maggi F, Tapondjou LA, Womeni HM, Quassinti L, Bramucci M, Vitali LA, Petrelli D, Lupidi G, Papa F, Vittori S, Barboni L (2014) Volatile oil from striped African pepper (Xylopia parviflora, Annonaceae) possesses notable chemopreventive, anti-inflammatory and antimicrobial potential. Food Chem 149:183–189

    Article  CAS  Google Scholar 

  • Yadav AK, Kim SH, Sun Chul Kang SC (2015) Chemical composition, antioxidant potential and cyto-protecting activity of essential oil of Liriodendron tulipifera L. Leaves, Kor. J Herbol 30:1–9

    Article  Google Scholar 

  • Zhou Y, Li M, Zhao F, Zha H, Yang L, Lu Y, Wang G, Shi J, Chen J (2016) floral nectary morphology and proteomic analysis of nectar of Liriodendron tulipifera Linn. Front. Plant Sci 7:826

    Google Scholar 

  • Zhu T, Xu Y, Dong B, Zhang J, Wei Z, Xu Y, Yao Y (2011) β-elemene inhibits proliferation of human glioblastoma cells through the activation of glia maturation factor β and induces sensitization to cisplatin. Oncol Rep 26:405–413

    CAS  Google Scholar 

  • Zihare L, Blumberga D (2017) Insight into bioeconomy. Solidago canadensis as a valid resource. Brief review. Energy Procedia 128:275–280

    Article  Google Scholar 

  • Zorzetto C, Sánchez-Mateo CC, Rabanal RM, Lupidi G, Petrelli D, Vitali LA, Bramucci M, Quassinti L, Caprioli G, Papa F, Ricciutelli M, Sagratini G, Vittori S, Maggi F (2015) Phytochemical analysis and in vitro biological activity of three Hypericum species from the Canary Islands (Hypericum reflexum, Hypericum canariense and Hypericum grandifolium). Fitoterapia 100:95–109

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Pharmacy, University of Camerino, Camerino, Italy

    Luana Quassinti, Filippo Maggi, Federica Ortolani, Giulio Lupidi, Luca A. Vitali & Massimo Bramucci

  2. School of Biosciences and Veterinary Medicine, University of Camerino, Camerino, Italy

    Dezemona Petrelli & Antonino Miano

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  1. Luana Quassinti
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  2. Filippo Maggi
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  3. Federica Ortolani
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  4. Giulio Lupidi
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Fig. 1S

GC-MS chromatograms of essential oils obtained from leaves (a: May and b: June), flowers (c) and fruits (d) of Liriodendron tulipifera. (PPTX 253 kb)

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Quassinti, L., Maggi, F., Ortolani, F. et al. Exploring new applications of tulip tree (Liriodendron tulipifera L.): leaf essential oil as apoptotic agent for human glioblastoma. Environ Sci Pollut Res 26, 30485–30497 (2019). https://doi.org/10.1007/s11356-019-06217-4

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