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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Caffeoylquinic Acids with Potential Biological Activity from Plant In vitro Cultures as Alternative Sources of Valuable Natural Products

Author(s): Ewa Skała*, Joanna Makowczyńska, Joanna Wieczfinska, Tomasz Kowalczyk and Przemysław Sitarek

Volume 26, Issue 24, 2020

Page: [2817 - 2842] Pages: 26

DOI: 10.2174/1381612826666200212115826

Price: $65

Abstract

Background: For a long time, the researchers have been looking for new efficient methods to enhance production and obtain valuable plant secondary metabolites, which would contribute to the protection of the natural environment through the preservation of various plant species, often rare and endangered. These possibilities offer plant in vitro cultures which can be performed under strictly-controlled conditions, regardless of the season or climate and environmental factors. Biotechnological methods are promising strategies for obtaining the valuable plant secondary metabolites with various classes of chemical compounds including caffeoylquinic acids (CQAs) and their derivatives. CQAs have been found in many plant species which are components in the daily diet and exhibit a wide spectrum of biological activities, including antioxidant, immunomodulatory, antihypertensive, analgesic, anti-inflammatory, hepato- and neuroprotective, anti-hyperglycemic, anticancer, antiviral and antimicrobial activities. They have also been found to offer protection against Alzheimer’s disease, and play a role in weight reduction and lipid metabolism control, as well as modulating the activity of glucose-6-phosphatase involved in glucose metabolism.

Methods: This work presents the review of the recent advances in use in vitro cultures of various plant species for the alternative system to the production of CQAs and their derivatives. Production of the secondary metabolites in in vitro culture is usually performed with cell suspension or organ cultures, such as shoots and adventitious or transformed roots. To achieve high production of valuable secondary metabolites in in vitro cultures, the optimization of the culture condition is necessary with respect to both biomass accumulation and metabolite content. The optimization of the culture conditions can be achieved by choosing the type of medium, growth regulators or growth conditions, selection of high-productivity lines or culture period, supplementation of the culture medium with precursors or elicitor treatments. Cultivation for large-scale in bioreactors and genetic engineering: Agrobacterium rhizogenes transformation and expression improvement of transcriptional factor or genes involved in the secondary metabolite production pathway are also efficient strategies for enhancement of the valuable secondary metabolites.

Results: Many studies have been reported to obtain highly productive plant in vitro cultures with respect to CQAs. Among these valuable secondary metabolites, the most abundant compound accumulated in in vitro cultures was 5-CQA (chlorogenic acid). Highly productive cultures with respect to this phenolic acid were Leonurus sibiricus AtPAP1 transgenic roots, Lonicera macranthoides and Eucomia ulmoides cell suspension cultures which accumulated above 20 mg g-1 DW 5-CQA. It is known that di- and triCQAs are less common in plants than monoCQAs, but it was also possible to obtain them by biotechnological methods.

Conclusion: The results indicate that the various in vitro cultures of different plant species can be a profitable approach for the production of CQAs. In particular, an efficient production of these valuable compounds is possible by Lonicera macranthoides and Eucomia ulmoides cell suspension cultures, Leonurus sibiricus transformed roots and AtPAP1 transgenic roots, Echinacea angustifolia adventitious shoots, Rhaponticum carthamoides transformed plants, Lavandula viridis shoots, Sausera involucrata cell suspension and Cichorium intybus transformed roots.

Keywords: Caffeoylquinic acids, plant in vitro cultures, biological activities, Alzheimer’s disease, Cultivation, triCQAs.

[1]
Del Rio D, Rodriguez-Mateos A, Spencer JPE, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 2013; 18(14): 1818-92.
[http://dx.doi.org/10.1089/ars.2012.4581] [PMID: 22794138]
[2]
Rodriguez-Mateos A, Vauzour D, Krueger CG, et al. Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update. Arch Toxicol 2014; 88(10): 1803-53.
[http://dx.doi.org/10.1007/s00204-014-1330-7] [PMID: 25182418]
[3]
Clifford MN, Jaganath IB, Ludwig IA, Crozier A. Chlorogenic acids and the acyl-quinic acids: discovery, biosynthesis, bioavailability and bioactivity. Nat Prod Rep 2017; 34(12): 1391-421.
[http://dx.doi.org/10.1039/C7NP00030H] [PMID: 29160894]
[4]
Chen K, Thomas SR, Keaney JF Jr. Beyond LDL oxidation: ROS in vascular signal transduction. Free Radic Biol Med 2003; 35(2): 117-32.
[http://dx.doi.org/10.1016/S0891-5849(03)00239-9] [PMID: 12853068]
[5]
Kolodziejczyk-Czepas J, Olas B, Malinowska J, et al. Trifolium pallidum and Trifolium scabrum extracts in the protection of human plasma components. J Thromb Thrombolysis 2013; 35(2): 193-9.
[http://dx.doi.org/10.1007/s11239-012-0792-9] [PMID: 23335023]
[6]
Perry G, Cash AD, Smith MA. Alzheimer disease and oxidative stress. J Biomed Biotechnol 2002; 2(3): 120-3.
[http://dx.doi.org/10.1155/S1110724302203010] [PMID: 12488575]
[7]
Pisoschi AM, Pop A. The role of antioxidants in the chemistry of oxidative stress: A review. Eur J Med Chem 2015; 97: 55-74.
[http://dx.doi.org/10.1016/j.ejmech.2015.04.040] [PMID: 25942353]
[8]
Szweda PA, Friguet B, Szweda LI. Proteolysis, free radicals, and aging. Free Radic Biol Med 2002; 33(1): 29-36.
[http://dx.doi.org/10.1016/S0891-5849(02)00837-7] [PMID: 12086679]
[9]
Sasaki K, Han J, Shigemori H, Isoda H. Caffeoylquinic acid induces ATP production and energy metabolism in human neurotypic SH-SY5Y cells. Nutr Aging (Amst) 2012; 1: 141-50.
[http://dx.doi.org/10.3233/NUA-2012-0012]
[10]
Gali-Muhtasib H, Hmadi R, Kareh M, Tohme R, Darwiche N. Cell death mechanisms of plant-derived anticancer drugs: beyond apoptosis. Apoptosis 2015; 20(12): 1531-62.
[http://dx.doi.org/10.1007/s10495-015-1169-2] [PMID: 26362468]
[11]
Bulgakov VP, Vereshchagina YV, Veremeichik GN. Anticancer polyphenols from cultured plant cells: production and new bioengineering strategies. Curr Med Chem 2018; 25(36): 4671-92.
[http://dx.doi.org/10.2174/0929867324666170609080357] [PMID: 28595545]
[12]
Dai J, Mumper RJ. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 2010; 15(10): 7313-52.
[http://dx.doi.org/10.3390/molecules15107313] [PMID: 20966876]
[13]
Mondolot L, La Fisca P, Buatois B, Talansier E, de Kochko A, Campa C. Evolution in caffeoylquinic acid content and histolocalization during Coffea canephora leaf development. Ann Bot 2006; 98(1): 33-40.
[http://dx.doi.org/10.1093/aob/mcl080] [PMID: 16675605]
[14]
Cheevarungnapakul K, Khaksar G, Panpetch P, Boonjing P, Sirikantaramas S. Identification and functional characterization of genes involved in the biosynthesis of caffeoylquinic acids in sunflower (Helianthus annuus L.). Front Plant Sci 2019; 10: 968.
[http://dx.doi.org/10.3389/fpls.2019.00968] [PMID: 31417585]
[15]
Kurata R, Adachi M, Yamakawa O, Yoshimoto M. Growth suppression of human cancer cells by polyphenolics from sweetpotato (Ipomoea batatas L.) leaves. J Agric Food Chem 2007; 55(1): 185-90.
[http://dx.doi.org/10.1021/jf0620259] [PMID: 17199331]
[16]
Truong VD, McFeeters RF, Thompson RT, Dean LL, Shofran B. Phenolic acid content and composition in leaves and roots of common commercial sweetpotato (Ipomea batatas L.) cultivars in the United States. J Food Sci 2007; 72(6): C343-9.
[http://dx.doi.org/10.1111/j.1750-3841.2007.00415.x] [PMID: 17995676]
[17]
Jeng TL, Lai CC, Liao TC, Lin SY, Sung JM. Effects of drying on caffeoylquinic acid derivative content and antioxidant capacity of sweet potato leaves. Yao Wu Shi Pin Fen Xi 2015; 23(4): 701-8.
[http://dx.doi.org/10.1016/j.jfda.2014.07.002] [PMID: 28911486]
[18]
Iwai K, Kishimoto N, Kakino Y, Mochida K, Fujita T. In vitro antioxidative effects and tyrosinase inhibitory activities of seven hydroxycinnamoyl derivatives in green coffee beans. J Agric Food Chem 2004; 52(15): 4893-8.
[http://dx.doi.org/10.1021/jf040048m] [PMID: 15264931]
[19]
Puangpraphant S, Berhow MA, Vermillion K, Potts G, Gonzalez de Mejia E. Dicaffeoylquinic acids in Yerba mate (Ilex paraguariensis St. Hilaire) inhibit NF-κB nucleus translocation in macrophages and induce apoptosis by activating caspases-8 and -3 in human colon cancer cells. Mol Nutr Food Res 2011; 55(10): 1509-22.
[http://dx.doi.org/10.1002/mnfr.201100128] [PMID: 21656672]
[20]
Stojakowska A, Malarz J, Szewczyk A, Kisiel W. Caffeic acid derivatives from a hairy root culture of Lactuca virosa. Acta Physiol Plant 2012; 34: 291-8.
[http://dx.doi.org/10.1007/s11738-011-0827-4]
[21]
Kim YK, Li X, Xu H, et al. Production of phenolic compounds in hairy root culture of tartary buckwheat (Fagopyrum tataricum Gaertn). J Crop Sci Biotechnol 2009; 12: 53-8.
[http://dx.doi.org/10.1007/s12892-009-0075-y]
[22]
Li Y, Chen M, Wang S, Ning J, Ding X, Chu Z. AtMYB11 regulates caffeoylquinic acid and flavonol synthesis in tomato and tobacco. Plant Cell Tissue Organ Cult 2015; 122: 309-19.
[http://dx.doi.org/10.1007/s11240-015-0767-6]
[23]
Al-Okbi SY, Mohamed DA, Gabr AMM, Mabrok HB, Hamed TE. Potential hepato- and reno-protective effect of artichoke callus culture and its alcohol extract in galactosamine hydrochloride treated rats. IJPPR 2017; 9: 415-23.
[http://dx.doi.org/10.25258/phyto.v9i2.8094]
[24]
Mubarak A, Bondonno CP, Liu AH, et al. Acute effects of chlorogenic acid on nitric oxide status, endothelial function, and blood pressure in healthy volunteers: a randomized trial. J Agric Food Chem 2012; 60(36): 9130-6.
[http://dx.doi.org/10.1021/jf303440j] [PMID: 22900702]
[25]
Olmos A, Giner RM, Recio MC, Ríos JL, Gil-Benso R, Máñez S. Interaction of dicaffeoylquinic derivatives with peroxynitrite and other reactive nitrogen species. Arch Biochem Biophys 2008; 475(1): 66-71.
[http://dx.doi.org/10.1016/j.abb.2008.04.012] [PMID: 18455492]
[26]
Malarz J, Stojakowska A, Kisiel W. Long-term cultured hairy roots of chicory-a rich source of hydroxycinnamates and 8-deoxylactucin glucoside. Appl Biochem Biotechnol 2013; 171(7): 1589-601.
[http://dx.doi.org/10.1007/s12010-013-0446-1] [PMID: 23975347]
[27]
Stojakowska A, Malarz J, Kiss AK. Hydroxycinnamates from elecampane (Inula helenium L.) callus culture. Acta Physiol Plant 2016; 38: 41.
[http://dx.doi.org/10.1007/s11738-016-2069-y]
[28]
Skała E, Kicel A, Olszewska MA, Kiss AK, Wysokińska H. Establishment of hairy root cultures of Rhaponticum carthamoides (Willd.) Iljin for the production of biomass and caffeic acid derivatives. BioMed Res Int 2015; 2015 181098: 11.
[http://dx.doi.org/10.1155/2015/181098]
[29]
Ncube EN, Mhlongo MI, Piater LA, Steenkamp PA, Dubery IA, Madala NE. Analyses of chlorogenic acids and related cinnamic acid derivatives from Nicotiana tabacum tissues with the aid of UPLC-QTOF-MS/MS based on the in-source collision-induced dissociation method. Chem Cent J 2014; 8(1): 66.
[http://dx.doi.org/10.1186/s13065-014-0066-z] [PMID: 25426160]
[30]
Zwyrzykowska A, Kupczyński R, Jarosz B, Szumny A, Kucharska AZ. Qualitative and quantitative analysis of polyphenolic compounds in Ilex sp. Open Chem 2015; 13: 1303-12.
[http://dx.doi.org/10.1515/chem-2015-0142]
[31]
Beckman C. Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defense responses in plants. Physiol Mol Plant Pathol 2000; 57: 101-10.
[http://dx.doi.org/10.1006/pmpp.2000.0287]
[32]
Martinez V, Mestre TC, Rubio F, et al. Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front Plant Sci 2016; 7: 838.
[http://dx.doi.org/10.3389/fpls.2016.00838] [PMID: 27379130]
[33]
Park H-J. Chemistry and pharmacological action of caffeoylquinic acid derivatives and pharmaceutical utilization of chwinamul (Korean Mountainous vegetable). Arch Pharm Res 2010; 33(11): 1703-20.
[http://dx.doi.org/10.1007/s12272-010-1101-9] [PMID: 21116772]
[34]
Moglia A, Lanteri S, Comino C, Acquadro A, de Vos R, Beekwilder J. Stress-induced biosynthesis of dicaffeoylquinic acids in globe artichoke. J Agric Food Chem 2008; 56(18): 8641-9.
[http://dx.doi.org/10.1021/jf801653w] [PMID: 18710252]
[35]
Vereshchagina YV, Bulgakov VP, Grigorchuk VP, et al. The rolC gene increases caffeoylquinic acid production in transformed artichoke cells. Appl Microbiol Biotechnol 2014; 98(18): 7773-80.
[http://dx.doi.org/10.1007/s00253-014-5869-2] [PMID: 24938208]
[36]
Xu J-G, Hu Q-P, Liu Y. Antioxidant and DNA-protective activities of chlorogenic acid isomers. J Agric Food Chem 2012; 60(46): 11625-30.
[http://dx.doi.org/10.1021/jf303771s] [PMID: 23134416]
[37]
Gil M, Wianowska D. Chlorogenic acids - their properties, occurrence and analysis 2017; 72: 61-104.
[http://dx.doi.org/10.17951/aa.2017.72.1.61]
[38]
Hong S, Joo T, Jhoo J-W. Antioxidant and anti-inflammatory activities of 3,5dicaffeoylquinic acid isolated from Ligularia fischeri leaves. Food Sci Biotechnol 2015; 24: 257-63.
[http://dx.doi.org/10.1007/s10068-015-0034-y]
[39]
Ohnishi M, Morishita H, Iwahashi H, et al. Inhibitory effects of chlorogenic acids on linoleic acid peroxidation and haemolysis. Phytochemistry 1994; 36: 579-83.
[http://dx.doi.org/10.1016/S0031-9422(00)89778-2]
[40]
Fraisse D, Felgines C, Texier O, Lamaison JL. Caffeoyl derivatives: major antioxidant compounds of some wild herbs of the Asteraceae family. Food Nutr Sci 2011; 2: 181-92.
[http://dx.doi.org/10.4236/fns.2011.230025]
[41]
Mijangos-Ramos IF, Zapata-Estrella HE, Ruiz-Vargas JA, et al. Bioactive dicaffeoylquinic acid derivatives from the root extract of Calea urticifolia. Rev Bras Farmacogn 2018; 28: 339-43.
[http://dx.doi.org/10.1016/j.bjp.2018.01.010]
[42]
Li X, Li K, Xie H, et al. Antioxidant and cytoprotective effects of the di-O-caffeoylquinic acid family: the mechanism, structure-activity relationship, and conformational effect. Molecules 2018; 23(1)E222
[http://dx.doi.org/10.3390/molecules23010222] [PMID: 29361719]
[43]
Garbetta A, Capotorto I, Cardinali A, et al. Antioxidant activity induced by main polyphenols present in edible artichoke heads: influence of in vitro gastro-intestinal digestion. J Funct Foods 2014; 10: 456-64.
[http://dx.doi.org/10.1016/j.jff.2014.07.019]
[44]
Cao X, Xiao H, Zhang Y, Zou L, Chu Y, Chu X. 1, 5-Dicaffeoylquinic acid-mediated glutathione synthesis through activation of Nrf2 protects against OGD/reperfusion-induced oxidative stress in astrocytes. Brain Res 2010; 1347: 142-8.
[http://dx.doi.org/10.1016/j.brainres.2010.05.072] [PMID: 20513363]
[45]
Zha R-P, Xu W, Wang W-Y, Dong L, Wang Y-P. Prevention of lipopolysaccharide-induced injury by 3,5-dicaffeoylquinic acid in endothelial cells. Acta Pharmacol Sin 2007; 28(8): 1143-8.
[http://dx.doi.org/10.1111/j.1745-7254.2007.00595.x] [PMID: 17640475]
[46]
Soh Y, Kim JA, Sohn NW, Lee KR, Kim SY. Protective effects of quinic acid derivatives on tetrahydropapaveroline-induced cell death in C6 glioma cells. Biol Pharm Bull 2003; 26(6): 803-7.
[http://dx.doi.org/10.1248/bpb.26.803] [PMID: 12808290]
[47]
Góngora L, Giner RM, Máñez S, Recio MdelC, Schinella G, Ríos JL. Effects of caffeoyl conjugates of isoprenyl-hydroquinone glucoside and quinic acid on leukocyte function. Life Sci 2002; 71(25): 2995-3004.
[http://dx.doi.org/10.1016/S0024-3205(02)02167-7] [PMID: 12384183]
[48]
Tatefuji T, Izumi N, Ohta T, Arai S, Ikeda M, Kurimoto M. Isolation and identification of compounds from Brazilian propolis which enhance macrophage spreading and mobility. Biol Pharm Bull 1996; 19(7): 966-70.
[http://dx.doi.org/10.1248/bpb.19.966] [PMID: 8839971]
[49]
Chen YL, Hwang TL, Yu HP, et al. Ilex kaushue and its bioactive component 3,5-dicaffeoylquinic acid protected mice from lipopolysaccharide-induced acute lung injury. Sci Rep 2016; 6: 34243.
[http://dx.doi.org/10.1038/srep34243] [PMID: 27681838]
[50]
Chen X, Miao J, Wang H, et al. The anti-inflammatory activities of Ainsliaea fragrans Champ. extract and its components in lipopolysaccharide-stimulated RAW264.7 macrophages through inhibition of NF-κB pathway. J Ethnopharmacol 2015; 170: 72-80.
[http://dx.doi.org/10.1016/j.jep.2015.05.004] [PMID: 25975516]
[51]
Shan J, Fu J, Zhao Z, et al. Chlorogenic acid inhibits lipopolysaccharide-induced cyclooxygenase-2 expression in RAW264.7 cells through suppressing NF-kappaB and JNK/AP-1 activation. Int Immunopharmacol 2009; 9(9): 1042-8.
[http://dx.doi.org/10.1016/j.intimp.2009.04.011] [PMID: 19393773]
[52]
dos Santos MD, Chen G, Almeida MC, et al. Effects of caffeoylquinic acid derivatives and C-flavonoid from Lychnophora ericoides on in vitro inflammatory mediator production. Nat Prod Commun 2010; 5(5): 733-40.
[http://dx.doi.org/10.1177/1934578X1000500512] [PMID: 20521538]
[53]
Abdel Motaal A, Ezzat SM, Tadros MG, El-Askary HI. In vivo anti-inflammatory activity of caffeoylquinic acid derivatives from Solidago virgaurea in rats. Pharm Biol 2016; 54(12): 2864-70.
[http://dx.doi.org/10.1080/13880209.2016.1190381] [PMID: 27249953]
[54]
Peluso G, De Feo V, De Simone F, Bresciano E, Vuotto ML. Studies on the inhibitory effects of caffeoylquinic acids on monocyte migration and superoxide ion production. J Nat Prod 1995; 58(5): 639-46.
[http://dx.doi.org/10.1021/np50119a001] [PMID: 7623043]
[55]
Srinivasan K, Muruganandan S, Lal J, Chandra S, Tandan SK, Prakash VR. Evaluation of anti-inflammatory activity of Pongamia pinnata leaves in rats. J Ethnopharmacol 2001; 78(2-3): 151-7.
[http://dx.doi.org/10.1016/S0378-8741(01)00333-6] [PMID: 11694360]
[56]
Matsui T, Ebuchi S, Fujise T, et al. Strong antihyperglycemic effects of water-soluble fraction of Brazilian propolis and its bioactive constituent, 3,4,5-tri-O-caffeoylquinic acid. Biol Pharm Bull 2004; 27(11): 1797-803.
[http://dx.doi.org/10.1248/bpb.27.1797] [PMID: 15516726]
[57]
Kurata R, Yahara S, Yamakawa O, Yoshimoto M. Simple high-yield purification of 3,4,5-Tri-O-caffeoylquinic acid from sweetpotato (Ipomoea batatas L.) leaf and its inhibitory effects on aldose reductase. Food Sci Technol Res 2011; 17: 87-92.
[http://dx.doi.org/10.3136/fstr.17.87]
[58]
Terashima S, Shimizu M, Horie S, Morita N. Studies on aldose reductase inhibitors from natural products. IV. Constituents and aldose reductase inhibitory effect of Chrysanthemum morifolium, Bixa orellana and Ipomoea batatas. Chem Pharm Bull (Tokyo) 1991; 39(12): 3346-7.
[http://dx.doi.org/10.1248/cpb.39.3346] [PMID: 1814628]
[59]
Yang B-B, Hong Z-W, Zhang Z, et al. Epalrestat, an aldose reductase inhibitor, restores erectile function in streptozocin-induced diabetic rats. Int J Impot Res 2019; 31(2): 97-104.
[http://dx.doi.org/10.1038/s41443-018-0075-x] [PMID: 30214006]
[60]
Tang WH, Martin KA, Hwa J. Aldose reductase, oxidative stress, and diabetic mellitus. Front Pharmacol 2012; 3: 87.
[http://dx.doi.org/10.3389/fphar.2012.00087] [PMID: 22582044]
[61]
Nishimura C, Yamaoka T, Mizutani M, Yamashita K, Akera T, Tanimoto T. Purification and characterization of the recombinant human aldose reductase expressed in baculovirus system. Biochim Biophys Acta 1991; 1078(2): 171-8.
[http://dx.doi.org/10.1016/0167-4838(91)99006-E] [PMID: 1905957]
[62]
Alonso-Castro AJ, Miranda-Torres AC, González-Chávez MM, Salazar-Olivo LA. Cecropia obtusifolia Bertol and its active compound, chlorogenic acid, stimulate 2-NBDglucose uptake in both insulin-sensitive and insulin-resistant 3T3 adipocytes. J Ethnopharmacol 2008; 120(3): 458-64.
[http://dx.doi.org/10.1016/j.jep.2008.09.019] [PMID: 18948178]
[63]
Zhang X, Wu C, Wu H, et al. Anti-hyperlipidemic effects and potential mechanisms of action of the caffeoylquinic acid-rich Pandanus tectorius fruit extract in hamsters fed a high fat-diet. PLoS One 2013; 8(4)e61922
[http://dx.doi.org/10.1371/journal.pone.0061922] [PMID: 23613974]
[64]
Tian Y, Cao X-X, Shang H, et al. Synthesis and in vitro evaluation of caffeoylquinic acid derivatives as potential hypolipidemic agents. Molecules 2019; 24(5): 964.
[http://dx.doi.org/10.3390/molecules24050964] [PMID: 30857274]
[65]
Liu H, Zhang X, Wu Ch, Wu H, Guo P, Xu X. Anti-hyperlipidemic caffeoylquinic acids from the fruits of Pandanus tectorius Soland. J Appl Pharm Sci 2013; 3: 016-9.
[http://dx.doi.org/10.7324/JAPS.2013.3803]
[66]
Wu C, Zhang X, Zhang X, et al. The caffeoylquinic acid-rich Pandanus tectorius fruit extract increases insulin sensitivity and regulates hepatic glucose and lipid metabolism in diabetic db/db mice. J Nutr Biochem 2014; 25(4): 412-9.
[http://dx.doi.org/10.1016/j.jnutbio.2013.12.002] [PMID: 24629909]
[67]
Wan CW, Wong CN, Pin WK, et al. Chlorogenic acid exhibits cholesterol lowering and fatty liver attenuating properties by up-regulating the gene expression of PPAR-α in hypercholesterolemic rats induced with a high-cholesterol diet. Phytother Res 2013; 27(4): 545-51.
[http://dx.doi.org/10.1002/ptr.4751] [PMID: 22674675]
[68]
Cho AS, Jeon SM, Kim MJ, et al. Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food Chem Toxicol 2010; 48(3): 937-43.
[http://dx.doi.org/10.1016/j.fct.2010.01.003] [PMID: 20064576]
[69]
Mishima S, Yoshida C, Akino S, Sakamoto T. Antihypertensive effects of Brazilian propolis: identification of caffeoylquinic acids as constituents involved in the hypotension in spontaneously hypertensive rats. Biol Pharm Bull 2005; 28(10): 1909-14.
[http://dx.doi.org/10.1248/bpb.28.1909] [PMID: 16204944]
[70]
Han J, Miyamae Y, Shigemori H, Isoda H. Neuroprotective effect of 3,5-di-O-caffeoylquinic acid on SH-SY5Y cells and senescence-accelerated-prone mice 8 through the up-regulation of phosphoglycerate kinase-1. Neuroscience 2010; 169(3): 1039-45.
[http://dx.doi.org/10.1016/j.neuroscience.2010.05.049] [PMID: 20570715]
[71]
Hur JY, Soh Y, Kim BH, et al. Neuroprotective and neurotrophic effects of quinic acids from Aster scaber in PC12 cells. Biol Pharm Bull 2001; 24(8): 921-4.
[http://dx.doi.org/10.1248/bpb.24.921] [PMID: 11510486]
[72]
Miyamae Y, Kurisu M, Han J, Isoda H, Shigemori H. Structure-activity relationship of caffeoylquinic acids on the accelerating activity on ATP production. Chem Pharm Bull (Tokyo) 2011; 59(4): 502-7.
[http://dx.doi.org/10.1248/cpb.59.502] [PMID: 21467684]
[73]
Gray NE, Morré J, Kelley J, et al. Caffeoylquinic acids in Centella asiatica protect against amyloid-β toxicity. J Alzheimers Dis 2014; 40(2): 359-73.
[http://dx.doi.org/10.3233/JAD-131913] [PMID: 24448790]
[74]
Deng L, Pushpitha K, Joseph C, et al. Amyloid b induces early changes in the ribosomal machinery, cytoskeletal organization and oxidative phosphorylation in retinal photoreceptor cells. Front Mol Neurosci 2019; 12: 24.
[http://dx.doi.org/10.3389/fnmol.2019.00024] [PMID: 30853886]
[75]
Xiao HB, Cao X, Wang L, et al. 1,5-dicaffeoylquinic acid protects primary neurons from amyloid β 1-42-induced apoptosis via PI3K/Akt signaling pathway. Chin Med J (Engl) 2011; 124(17): 2628-35.
[PMID: 22040415]
[76]
Nakajima Y, Shimazawa M, Mishima S, Hara H. Water extract of propolis and its main constituents, caffeoylquinic acid derivatives, exert neuroprotective effects via antioxidant actions. Life Sci 2007; 80(4): 370-7.
[http://dx.doi.org/10.1016/j.lfs.2006.09.017] [PMID: 17046025]
[77]
Yanqin Y, Shaohua C, Jing T, Nan L. Caffeoylquinic acid enhances proliferation of oligodendrocyte precursor cells. Transl Neurosci 2017; 8: 111-6.
[http://dx.doi.org/10.1515/tnsci-2017-0017] [PMID: 29104800]
[78]
Choi J, Park JK, Lee KT, et al. Inhibitory effect of Ligularia fischeri var. spiciformis and its active component, 4,4-dicaffeoulquinic acid on the hepatic lipid peroxidation in acetaminophen-treated rat. Nat Prod Sci 2004; 10: 182-9.
[79]
An RB, Sohn DH, Jeong GS, Kim YC. In vitro hepatoprotective compounds from Suaeda glauca. Arch Pharm Res 2008; 31(5): 594-7.
[http://dx.doi.org/10.1007/s12272-001-1198-1] [PMID: 18481014]
[80]
Wang C, Wang G, Liu H, Hou YL. Protective effect of bioactive compounds from Lonicera japonica Thunb. against H2O2-induced cytotoxicity using neonatal rat cardiomyocytes. Iran J Basic Med Sci 2016; 19(1): 97-105.
[PMID: 27096070]
[81]
Fiamegos YC, Kastritis PL, Exarchou V, et al. Antimicrobial and efflux pump inhibitory activity of caffeoylquinic acids from Artemisia absinthium against gram-positive pathogenic bacteria. PLoS One 2011; 6(4)e18127
[http://dx.doi.org/10.1371/journal.pone.0018127] [PMID: 21483731]
[82]
Zhu X, Zhang H, Lo R. Phenolic compounds from the leaf extract of artichoke (Cynara scolymus L.) and their antimicrobial activities. J Agric Food Chem 2004; 52(24): 7272-8.
[http://dx.doi.org/10.1021/jf0490192] [PMID: 15563206]
[83]
Harrison HF Jr, Mitchell TR, Peterson JK, Wechter WP, Majetich GF, Snook ME. Contents of caffeoylquinic acid compounds in the storage roots of sixteen sweetpotato genotypes and their potential biological activity. J Am Soc Hortic Sci 2008; 133: 492-500.
[http://dx.doi.org/10.21273/JASHS.133.4.492]
[84]
Stange RR Jr, Midland SL, Holmes GJ, Sims JJ, Mayer RT. Constituents from the periderm and outer cortex of Ipomoeahataras with antifungal activity against Rhizopus stolonifer. Postharvest Biol Technol 2001; 23: 85-92.
[http://dx.doi.org/10.1016/S0925-5214(01)00105-3]
[85]
Mahmood N, Moore PS, De Tommasi N, et al. Inhibition of HIV infection by caffeoylquinic acid derivatives. Antivir Chem Chemother 1993; 4: 235-40.
[http://dx.doi.org/10.1177/095632029300400406]
[86]
Zhu K, Cordeiro ML, Atienza J, Robinson WE Jr, Chow SA. Irreversible inhibition of human immunodeficiency virus type 1 integrase by dicaffeoylquinic acids. J Virol 1999; 73(4): 3309-16.
[PMID: 10074185]
[87]
Kwon HC, Jung CM, Shin CG, et al. A new caffeoyl quinic acid from aster scaber and its inhibitory activity against human immunodeficiency virus-1 (HIV-1) integrase. Chem Pharm Bull (Tokyo) 2000; 48(11): 1796-8.
[http://dx.doi.org/10.1248/cpb.48.1796] [PMID: 11086919]
[88]
Tamura H, Akioka T, Ueno K, et al. Anti-human immunodeficiency virus activity of 3,4,5-tricaffeoylquinic acid in cultured cells of lettuce leaves. Mol Nutr Food Res 2006; 50(4-5): 396-400.
[http://dx.doi.org/10.1002/mnfr.200500216] [PMID: 16598806]
[89]
Hu Z, Chen D, Dong L, Southerland WM. Prediction of the interaction of HIV-1 integrase and its dicaffeoylquinic acid inhibitor through molecular modeling approach. Ethn Dis 2010; 20: 1-45-9.
[90]
Heyman HM, Senejoux F, Seibert I, Klimkait T, Maharaj VJ, Meyer JJM. Identification of anti-HIV active dicaffeoylquinic- and tricaffeoylquinic acids in Helichrysum populifolium by NMR-based metabolomic guided fractionation. Fitoterapia 2015; 103: 155-64.
[http://dx.doi.org/10.1016/j.fitote.2015.03.024] [PMID: 25841639]
[91]
Serina JC, Castilho PC, Fernandes MX. Caffeoylquinic acids as inhibitors for HIV-I protease and HIV-I Integrase. A molecular docking study. SDRP J Comp Chem Molecular Modelling 2016; 1: 34-7.
[92]
Li Y, But PPH, Ooi VEC. Antiviral activity and mode of action of caffeoylquinic acids from Schefflera heptaphylla (L.) Frodin. Antiviral Res 2005; 68(1): 1-9.
[http://dx.doi.org/10.1016/j.antiviral.2005.06.004] [PMID: 16140400]
[93]
Takemura T, Urushisaki T, Fukuoka M, et al. 3,4-Dicaffeoylquinic acid, a major constituent of brazilian propolis, increases TRAIL expression and extends the lifetimes of mice infected with the influenza A virus. Evid Based Complement Alternat Med 2012.9468677
[http://dx.doi.org/10.1155/2012/946867]
[94]
Urushisaki T, Takemura T, Tazawa S, et al. Caffeoylquinic acids are major constituents with potent anti-influenza effects in brazilian green propolis water extract. Evid Based Complement Alternat Med 2011. 254914
[http://dx.doi.org/10.1155/2011/254914]
[95]
Zhao Y, Geng CA, Ma YB, et al. UFLC/MS-IT-TOF guided isolation of anti-HBV active chlorogenic acid analogues from Artemisia capillaris as a traditional Chinese herb for the treatment of hepatitis. J Ethnopharmacol 2014; 156: 147-54.
[http://dx.doi.org/10.1016/j.jep.2014.08.043] [PMID: 25219603]
[96]
Ge L, Wan H, Tang S, et al. Novel caffeoylquinic acid derivatives from Lonicera japonica Thunb. flower buds exert pronounced anti-HBV activities. RSC Advances 2018; 8: 35374-85.
[http://dx.doi.org/10.1039/C8RA07549B]
[97]
dos Santos MD, Gobbo-Neto L, Albarella L, de Souza GE, Lopes NP. Analgesic activity of di-caffeoylquinic acids from roots of Lychnophora ericoides (Arnica da serra). J Ethnopharmacol 2005; 96(3): 545-9.
[http://dx.doi.org/10.1016/j.jep.2004.09.043] [PMID: 15619576]
[98]
Choi SZ, Choi SU, Lee KR. Phytochemical constituents of the aerial parts from Solidago virga-aurea var. gigantea. Arch Pharm Res 2004; 27(2): 164-8.
[http://dx.doi.org/10.1007/BF02980100] [PMID: 15022716]
[99]
Teoh WY, Wahab NA, Sim KS. Caffeoylquinic acids induce cell death and cell cycle arrest on HCT 116 cells via formation of extracellular H2O2 and quinones. Warasan Khana Witthayasat Maha Witthayalai Chiang Mai 2018; 45: 318-30.
[100]
Rakshit S, Mandal L, Pal BC, et al. Involvement of ROS in chlorogenic acid-induced apoptosis of Bcr-Abl+ CML cells. Biochem Pharmacol 2010; 80(11): 1662-75.
[http://dx.doi.org/10.1016/j.bcp.2010.08.013] [PMID: 20832390]
[101]
Yang J-S, Liu C-W, Ma Y-S, et al. Chlorogenic acid induces apoptotic cell death in U937 leukemia cells through caspase- and mitochondria-dependent pathways. In Vivo 2012; 26(6): 971-8.
[PMID: 23160680]
[102]
Mishima S, Inoh Y, Narita Y, et al. Identification of caffeoylquinic acid derivatives from Brazilian propolis as constituents involved in induction of granulocytic differentiation of HL-60 cells. Bioorg Med Chem 2005; 13(20): 5814-8.
[http://dx.doi.org/10.1016/j.bmc.2005.05.044] [PMID: 15993085]
[103]
Facino RM, Carini M, Aldini G, Saibene L, Pietta P, Mauri P. Echinacoside and caffeoyl conjugates protect collagen from free radical-induced degradation: a potential use of Echinacea extracts in the prevention of skin photodamage. Planta Med 1995; 61(6): 510-4.
[http://dx.doi.org/10.1055/s-2006-959359] [PMID: 8824943]
[104]
Kitagawa S, Yoshii K, Morita SY, Teraoka R. Efficient topical delivery of chlorogenic acid by an oil-in-water microemulsion to protect skin against UV-induced damage. Chem Pharm Bull (Tokyo) 2011; 59(6): 793-6.
[http://dx.doi.org/10.1248/cpb.59.793] [PMID: 21628922]
[105]
Dong G-C, Chuang P-H, Chang K-C, et al. Blocking effect of an immuno-suppressive agent, cynarin, on CD28 of T-cell receptor. Pharm Res 2009; 26(2): 375-81.
[http://dx.doi.org/10.1007/s11095-008-9754-5] [PMID: 18989760]
[106]
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39(1): 44-84.
[http://dx.doi.org/10.1016/j.biocel.2006.07.001] [PMID: 16978905]
[107]
Beal MF. Energetics in the pathogenesis of neurodegenerative diseases. Trends Neurosci 2000; 23(7): 298-304.
[http://dx.doi.org/10.1016/S0166-2236(00)01584-8] [PMID: 10856939]
[108]
Orth M, Schapira AH. Mitochondria and degenerative disorders. Am J Med Genet 2001; 106(1): 27-36.
[http://dx.doi.org/10.1002/ajmg.1425] [PMID: 11579422]
[109]
Moro MA, Almeida A, Bolaños JP, Lizasoain I. Mitochondrial respiratory chain and free radical generation in stroke. Free Radic Biol Med 2005; 39(10): 1291-304.
[http://dx.doi.org/10.1016/j.freeradbiomed.2005.07.010] [PMID: 16257638]
[110]
Van Houten B, Woshner V, Santos JH. Role of mitochondrial DNA in toxic responses to oxidative stress. DNA Repair (Amst) 2006; 5(2): 145-52.
[http://dx.doi.org/10.1016/j.dnarep.2005.03.002] [PMID: 15878696]
[111]
Kimura Y, Okuda H, Okuda T, Hatano T, Agata I, Arichi S. Studies on the activities of tannins and related compounds from medicinal plants and drugs. VI. Inhibitory effects of caffeoylquinic acids on histamine release from rat peritoneal mast cells. Chem Pharm Bull (Tokyo) 1985; 33(2): 690-6.
[http://dx.doi.org/10.1248/cpb.33.690] [PMID: 2410155]
[112]
Jiang Y, Kusama K, Satoh K, Takayama E, Watanabe S, Sakagami H. Induction of cytotoxicity by chlorogenic acid in human oral tumor cell lines. Phytomedicine 2000; 7(6): 483-91.
[http://dx.doi.org/10.1016/S0944-7113(00)80034-3] [PMID: 11194177]
[113]
Weng CJ, Yen GC. Chemopreventive effects of dietary phytochemicals against cancer invasion and metastasis: phenolic acids, monophenol, polyphenol, and their derivatives. Cancer Treat Rev 2012; 38(1): 76-87.
[http://dx.doi.org/10.1016/j.ctrv.2011.03.001] [PMID: 21481535]
[114]
Taira J, Uehara M, Tsuchida E, Ohmine W. Inhibition of the β-catenin/Tcf signaling by caffeoylquinic acids in sweet potato leaf through down regulation of the Tcf-4 transcription. J Agric Food Chem 2014; 62(1): 167-72.
[http://dx.doi.org/10.1021/jf404411r] [PMID: 24308429]
[115]
Yoshimoto M, Yahara S, Okuno S, Islam MS, Ishiguro K, Yamakawa O. Antimutagenicity of mono-, di-, and tricaffeoylquinic acid derivatives isolated from sweetpotato (Ipomoea batatas L.) leaf. Biosci Biotechnol Biochem 2002; 66(11): 2336-41.
[http://dx.doi.org/10.1271/bbb.66.2336] [PMID: 12506969]
[116]
In JK, Kim JK, Oh JS, Seo DW. 5-Caffeoylquinic acid inhibits invasion of non-small cell lung cancer cells through the inactivation of p70S6K and Akt activity: Involvement of p53 in differential regulation of signaling pathways. Int J Oncol 2016; 48(5): 1907-12.
[http://dx.doi.org/10.3892/ijo.2016.3436] [PMID: 26984670]
[117]
Jin UH, Lee JY, Kang SK, et al. A phenolic compound, 5-caffeoylquinic acid (chlorogenic acid), is a new type and strong matrix metalloproteinase-9 inhibitor: isolation and identification from methanol extract of Euonymus alatus. Life Sci 2005; 77(22): 2760-9.
[http://dx.doi.org/10.1016/j.lfs.2005.02.028] [PMID: 16005473]
[118]
Bandyopadhyay G, Biswas T, Roy KC, et al. Chlorogenic acid inhibits Bcr-Abl tyrosine kinase and triggers p38 mitogen-activated protein kinase-dependent apoptosis in chronic myelogenous leukemic cells. Blood 2004; 104(8): 2514-22.
[http://dx.doi.org/10.1182/blood-2003-11-4065] [PMID: 15226183]
[119]
Xue N, Zhou Q, Ji M, et al. Chlorogenic acid inhibits glioblastoma growth through repolarizating macrophage from M2 to M1 phenotype. Sci Rep 2017; 7: 39011.
[http://dx.doi.org/10.1038/srep39011] [PMID: 28045028]
[120]
Yoon MH, Cho CW, Lee JH, Kim YS, An GH, Lim CH. Antithrombotic compounds from the leaves of Ligularia stenocephala M. Nat Prod Sci 2008; 14: 62-7.
[121]
Satake T, Kamiya K, An Y, Oishi Nee Taka T, Yamamoto J. The anti-thrombotic active constituents from Centella asiatica. Biol Pharm Bull 2007; 30(5): 935-40.
[http://dx.doi.org/10.1248/bpb.30.935] [PMID: 17473438]
[122]
Dias MI, Sousa MJ, Alves RC, Ferreira ICFR. Exploring plant tissue culture to improve the production of phenoliccompounds: A review. Ind Crops Prod 2016; 82: 9-22.
[http://dx.doi.org/10.1016/j.indcrop.2015.12.016]
[123]
Smetanska I. Production of secondary metabolites using plant cell cultures. Adv Biochem Engin/Biotechnol 2008; 111: 187-228.
[http://dx.doi.org/10.1007/10_2008_103]
[124]
Rao SR, Ravishankar GA. Plant cell cultures: Chemical factories of secondary metabolites. Biotechnol Adv 2002; 20(2): 101-53.
[http://dx.doi.org/10.1016/S0734-9750(02)00007-1] [PMID: 14538059]
[125]
Gonçalves S, Romano A. Production of plant secondary metabolites by using biotechnological tools. In: Ramasamy Vijayakumar, Suresh SS Raja, Eds. Secondary metabolites - sources and applications IntechOpen. 2018.Available from:. https://www.intechopen.com/books/secondary-metabolites-sources-and-applications/production-of-plant-secondary-metabolites-by-using-biotechnological-tools
[http://dx.doi.org/10.5772/intechopen.76414]
[126]
Karuppusamy. A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plants Res 2009; 3: 1222-39.
[127]
Fujita Y, Tabata M. Secondary metabolites from plant cells: pharmaceutical applications and progress in commercial production. In: Green CE, Somers DA, Hackett WP, Biesboer DD, Eds. Plant Tissue and Cell Culture. New York: Alan R. Liss 1987; pp. 169-85.
[128]
Roychowdhury D, Majumder A, Jha S. Agrobacterium rhizogenesmediated transformation in medicinal plants: prospects and challenges. chapter 2, In: Chandra S, Lata H, Varma A, Eds. Biotechnology for Medicinal Plants, Micropropagation and Improvement. XVI, Hardcover, Springer-Verlag Berlin Heidelberg 2013; pp. 29-68.
[http://dx.doi.org/10.1007/978-3-642-29974-2_2]
[129]
Trumbo JL, Zhang B, Stewart CN Jr. Manipulating microRNAs for improved biomass and biofuels from plant feedstocks. Plant Biotechnol J 2015; 13(3): 337-54.
[http://dx.doi.org/10.1111/pbi.12319] [PMID: 25707745]
[130]
Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 2011; 23(4): 1512-22.
[http://dx.doi.org/10.1105/tpc.111.084525] [PMID: 21487097]
[131]
Kikowska M, Włodarczyk A, Stochmal A, Żuchowski J, Thiem B. Pentacyclic triterpenoids and polyphenols accumulation in cell suspension culture of Chaenomeles japonica (Thunb.) Lindl. ex Spach. Herba Pol 2019; 65: 1-11.
[http://dx.doi.org/10.2478/hepo-2019-0002]
[132]
Malarz J, Stojakowska A, Kisiel W. Sesquiterpene lactones in a hairy root culture of Cichorium intybus. Z Natforsch C J Biosci 2002; 57(11-12): 994-7.
[http://dx.doi.org/10.1515/znc-2002-11-1207] [PMID: 12562083]
[133]
Trajtemberg SP, Apostolo NM, Fernandez G. Calluses of Cynara cardunculus var. cardunculus Cardoon (Asteraceae): determination of cynarine and chlorogenic acid by automated high-performance capillary electrophoresis. In Vitro Cell Dev Biol Plant 2006; 42: 534-7.
[http://dx.doi.org/10.1079/IVP2006803]
[134]
Menin B, Moglia A, Comino C, Hakkert JC, Lanteri S, Beekwilder J. In vitro callus-induction in globe artichoke (Cynara cardunculus L.var. scolymus) as a system for the production of caffeoylquinic acids J Horti Sci Biotech 2013; 88: 537.
[http://dx.doi.org/10.1080/14620316.2013.11513003]
[135]
Liu W, Liu C, Yang C, Wang L, Li S. Effect of grape genotype and tissue type on callus growth and production of resveratrols and their piceids after UV-C irradiation. Food Chem 2010; 122: 475-81.
[http://dx.doi.org/10.1016/j.foodchem.2010.03.055]
[136]
Joshaghani MS, Ghasemnezhad A, Alizadeh M, Tanuri A. Assessment of some phenolic acids of artichoke callus under in vitro conditions. Iran J Plant Physiol 2014; 4: 1151-8.
[http://dx.doi.org/10.22034/IJPP.2014.540660]
[137]
El-Bahr MK, Bekheet SAE-H, Gabr AMM, El-Shenawy R, Abd YSE. Research article accumulation of cynarin, the hepatoprotective compound, in ethephon treated callus cultures of globe artichoke (Cynara scolymus L.). J Biol Sci 2018; 18: 243-50.
[http://dx.doi.org/10.3923/jbs.2018.243.250]
[138]
Kikowska M, Kędziora I, Krawczyk A, Thiem B. Methyl jasmonate, yeast extract and sucrose stimulate phenolic acids accumulation in Eryngium planum L. shoot cultures. Acta Biochim Pol 2015; 62(2): 197-200.
[http://dx.doi.org/10.18388/abp.2014_880] [PMID: 25856557]
[139]
Lucchesini M, Bertoli A, Mensuali-Sodi A, Pistelli L. Establishment of in vitro tissue cultures from Echinacea angustifolia D.C. adult plants for the production of phytochemical compounds. Sci Hortic (Amsterdam) 2009; 122: 484-90.
[http://dx.doi.org/10.1016/j.scienta.2009.06.011]
[140]
Cui H-Y. Abdullahil Baque Md, Lee E-J, Paek K-Y. Scale-up of adventitious root cultures of Echinacea angustifolia in a pilot-scale bioreactor for the production of biomass and caffeic acid derivatives. Plant Biotechnol Rep 2013; 7: 297-308.
[http://dx.doi.org/10.1007/s11816-012-0263-y]
[141]
Wu C-H, Murthy HN, Hahn E-J, Paek K-Y. Enhanced production of caftaric acid, chlorogenic acid and cichoric acid in suspension cultures of Echinacea purpurea by the manipulation of incubation temperature and photoperiod. Biochem Eng J 2007; 36: 301-3.
[http://dx.doi.org/10.1016/j.bej.2007.02.024]
[142]
Wu C-H, Murthy HN, Hahn E-J, Paek K-Y. Improved production of caffeic acid derivatives in suspension cultures of Echinacea purpurea by medium replenishment strategy. Arch Pharm Res 2007; 30(8): 945-9.
[http://dx.doi.org/10.1007/BF02993961] [PMID: 17879746]
[143]
Wu C-H, Murthy HN, Hahn E-J, Paek K-Y. Large-scale cultivation of adventitious roots of Echinacea purpurea in airlift bioreactors for the production of chichoric acid, chlorogenic acid and caftaric acid. Biotechnol Lett 2007; 29(8): 1179-82.
[http://dx.doi.org/10.1007/s10529-007-9399-1] [PMID: 17589811]
[144]
Jeong J-A, Wu C-H, Murthy HN, Hahn E-J, Paek K-Y. Application of an airlift bioreactor system for production of adventitious root biomass and caffeic acid derivatives of Echinacea purpurea. Biotechnol Bioproc E 2009; 14: 91-8.
[http://dx.doi.org/10.1007/s12257-007-0142-5]
[145]
Liu C-Z, Abbasi BH, Gao M, Murch SJ, Saxena PK. Caffeic acid derivatives production by hairy root cultures of Echinacea purpurea. J Agric Food Chem 2006; 54(22): 8456-60.
[http://dx.doi.org/10.1021/jf061940r] [PMID: 17061821]
[146]
Abbasi BH, Tian C-L, Murch SJ, Saxena PK, Liu C-Z. Light-enhanced caffeic acid derivatives biosynthesis in hairy root cultures of Echinacea purpurea. Plant Cell Rep 2007; 26(8): 1367-72.
[http://dx.doi.org/10.1007/s00299-007-0344-5] [PMID: 17396238]
[147]
Kikowska M, Budzianowski J, Krawczyk A, Thiem B. Accumulation of rosmarinic, chlorogenic and caffeic acids in in vitro cultures of Eryngium planum L. Acta Physiol Plant 2012; 34: 2425-33.
[http://dx.doi.org/10.1007/s11738-012-1011-1]
[148]
Kikowska M, Thiem B, Sliwinska E, et al. The effect of nutritional factors and plant growth regulators on micropropagation and production of phenolic acids and saponins from plantlets and adventitious root cultures of Eryngium maritimum L. J Plant Growth Regul 2014; 33: 809-19.
[http://dx.doi.org/10.1007/s00344-014-9428-y]
[149]
Wang J, Liao X, Zhang H, Du J, Chen P. Accumulation of chlorogenic acid in cell suspension cultures of Eucommia ulmoides. Plant Cell Tissue Organ Cult 2003; 74: 193-5.
[http://dx.doi.org/10.1023/A:1023957129569]
[150]
Park NI, Li X, Uddin MR, Park SU. Phenolic compound production by different morphological phenotypes in hairy root cultures of Fagopyrum tataricum Gaertn. Arch Biol Sci 2011; 63: 193-8.
[http://dx.doi.org/10.2298/ABS1101193P]
[151]
Thiruvengadam M, Praveen N, Kim E-H, Kim S-H, Chung I-M. Production of anthraquinones, phenolic compounds and biological activities from hairy root cultures of Polygonum multiflorum Thunb. Protoplasma 2014; 251(3): 555-66.
[http://dx.doi.org/10.1007/s00709-013-0554-3] [PMID: 24091894]
[152]
Lin P, Yin ZP, Chen JG, Wu S. Effects of different culture conditions on callus growth and chlorogenic acid accumulation in Gardenia jasminoides Ellis. Xiandai Shipin Keji 2017; 33: 181-8.
[153]
Liu Z-B, Chen J-G, Yin Z-P, et al. Methyl jasmonate and salicylic acid elicitation increase content and yield of chlorogenic acid and its derivatives in Gardenia jasminoides cell suspension cultures. Plant Cell Tissue Organ Cult 2018; 134: 79-93.
[http://dx.doi.org/10.1007/s11240-018-1401-1]
[154]
Murthy HN, Lee E-J, Paek K-Y. Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tissue Organ Cult 2014; 118: 1-16.
[http://dx.doi.org/10.1007/s11240-014-0467-7]
[155]
Konczak-Islam I, Okuno S, Yoshimoto M, Yamakawa O. Composition of phenolics and anthocyanins in a sweet potato cell suspension culture. Biochem Eng J 2003; 14: 155-61.
[http://dx.doi.org/10.1016/S1369-703X(02)00216-4]
[156]
Konczak I, Okuno S, Yoshimoto M, Yamakawa O. Caffeoylquinic acids generated in vitro in a high-anthocyanin-accumulating sweet potato cell line. J Biomed Biotechnol 2004; 2004(5): 287-92.
[http://dx.doi.org/10.1155/S1110724304404069] [PMID: 15577191]
[157]
Yi TG, Park Y, Park J-E, Park NI. Enhancement of phenolic compounds and antioxidative activities by the combination of culture medium and methyl jasmonate elicitation in hairy root cultures of Lactuca indica L. Nat Prod Commun 2019; 1-9.
[http://dx.doi.org/10.1177/1934578X19861867]
[158]
Costa P, Gonçalves S, Valentão P, Andrade PB, Romano A. Accumulation of phenolic compounds in in vitro cultures and wild plants of Lavandula viridis L’Hér and their antioxidant and anti-cholinesterase potential. Food Chem Toxicol 2013; 57: 69-74.
[http://dx.doi.org/10.1016/j.fct.2013.03.006] [PMID: 23524312]
[159]
Sitarek P, Skała E, Toma M, et al. A preliminary study of apoptosis induction in glioma cells via alteration of the Bax/Bcl-2-p53 axis by transformed and non-transformed root extracts of Leonurus sibiricus L. Tumour Biol 2016; 37(7): 8753-64.
[http://dx.doi.org/10.1007/s13277-015-4714-2] [PMID: 26743778]
[160]
Sitarek P, Kowalczyk T, Rijo P, et al. Over-expression of AtPAP1 transcriptional factor enhances phenolic acid production in transgenic roots of Leonurus sibiricus L. and their biological activities. Mol Biotechnol 2018; 60(1): 74-82.
[http://dx.doi.org/10.1007/s12033-017-0048-1] [PMID: 29196986]
[161]
Qiu J, Sun S, Luo S, et al. Arabidopsis AtPAP1 transcription factor induces anthocyanin production in transgenic Taraxacum brevicorniculatum. Plant Cell Rep 2014; 33(4): 669-80.
[http://dx.doi.org/10.1007/s00299-014-1585-8] [PMID: 24556963]
[162]
Sitarek P, Kowalczyk T, Picot L, et al. Growth of Leonurus sibiricus L. roots with over-expression of AtPAP1 transcriptional factor in closed bioreactor, production of bioactive phenolic compounds and evaluation of their biological activity. Ind Crops Prod 2018; 122: 732-9.
[http://dx.doi.org/10.1016/j.indcrop.2018.06.059]
[163]
Sitarek P, Skała E, Toma M, et al. Transformed root extract of Leonurus sibiricus induces apoptosis through intrinsic and extrinsic pathways in various grades of human glioma cells. Pathol Oncol Res 2017; 23(3): 679-87.
[http://dx.doi.org/10.1007/s12253-016-0170-6] [PMID: 28032310]
[164]
Li Q, Tang M, Tan Y, Ma D, Wang Y, Zhang H. Improved production of chlorogenic acid from cell suspension cultures of Lonicera macranthoids. Trop J Pharm Res 2016; 15: 919-27.
[http://dx.doi.org/10.4314/tjpr.v15i5.4]
[165]
Śliwińska AA, Sykłowska-Baranek K, Kośmider A, et al. Stimulation of phenolic compounds production in the in vitro cultivated Polyscias filicifolia Bailey shoots and evaluation of the antioxidant and cytotoxic potential of plant extracts. Acta Soc Bot Pol 2018; 87: 3586.
[http://dx.doi.org/10.5586/asbp.3586]
[166]
Skała E, Picot L, Bijak M, et al. An efficient plant regeneration from Rhaponticum carthamoides transformed roots, enhanced caffeoylquinic acid derivatives production in pRi-transformed plants and their biological activity. Ind Crops Prod 2019; 129: 327-38.
[http://dx.doi.org/10.1016/j.indcrop.2018.12.020]
[167]
Skała E, Grąbkowska R, Sitarek P, Kuźma Ł, Błauż A, Wysokińska H. Rhaponticum carthamoides regeneration through direct and indirect organogenesis, molecular profiles and secondary metabolite production. Plant Cell Tissue Organ Cult 2015; 123: 83-98.
[http://dx.doi.org/10.1007/s11240-015-0816-1]
[168]
Chen R, Liu X, Zou J, Yang L, Dai J. Qualitative and quantitative analysis of phenylpropanoids in cell culture, regenerated plantlets and herbs of Saussurea involucrata. J Pharm Biomed Anal 2013; 74: 39-46.
[http://dx.doi.org/10.1016/j.jpba.2012.10.010] [PMID: 23245231]
[169]
Qiu J, Gao F, Shen G, et al. Metabolic engineering of the phenylpropanoid pathway enhances the antioxidant capacity of Saussurea involucrata. PLoS One 2013; 8(8)e70665
[http://dx.doi.org/10.1371/journal.pone.0070665] [PMID: 23976949]
[170]
Thiem B, Wesołowska M, Skrzypczak L, Budzianowski J. Phenolic compounds in two Solidago L. species from in vitro culture. Acta Pol Pharm 2001; 58(4): 277-81.
[PMID: 11693733]
[171]
Nieto-Trujillo A, Buend’ıa-Gonz’alez L, Garc’ıa-Morales C, Rom’an-Guerrero A, Cruz-Sosa F, Estrada-Z’u˜niga ME. Phenolic compounds and parthenolide production from in vitro cultures of Tanacetum parthenium. Rev Mex Ing Quim 2017; 16: 371-83.
[172]
Gamborg OL, Miller RA, Ojima K. Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 1968; 50(1): 151-8.
[http://dx.doi.org/10.1016/0014-4827(68)90403-5] [PMID: 5650857]
[173]
Linsmaier EM, Skoog F. Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 1965; 18: 100-27.
[http://dx.doi.org/10.1111/j.1399-3054.1965.tb06874.x]
[174]
Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 1962; 15: 473-97.
[http://dx.doi.org/10.1111/j.1399-3054.1962.tb08052.x]
[175]
Schenk RU, Hildebrandt AC. Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 1972; 50: 199-204.
[http://dx.doi.org/10.1139/b72-026]
[176]
Lloyd GB, McCown BH. Commercially-feasiblemicropropagation of mountain lamel Kalmia latifolia by use of shoottip culture. Proceedings of the International Plant Propagator’s Society 1980; 30: 421-7.

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