Skip to main content

Advertisement

SpringerLink
Log in

Characterization of lipid droplets from a Taxus media cell suspension and their potential involvement in trafficking and secretion of paclitaxel

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Our paper describes the potential roles of lipid droplets of Taxus media cell suspension in the biosynthesis and secretion of paclitaxel and, therefore, highlights their involvement in improving its production.

Abstract

Paclitaxel (PTX) is a highly potent anticancer drug that is mainly produced using Taxus sp. cell suspension cultures. The main purpose of the current study is to characterize cellular LDs from T. media cell suspension with a particular focus on the biological connection of their associated proteins, the caleosins (CLOs), with the biosynthesis and secretion of PTX. A pure LD fraction obtained from T. media cells and characterized in terms of their proteome. Interestingly, the cellular LD in T. media sequester the PTX. This was confirmed in vitro, where about 96% of PTX (C0PTX,aq [mg L−1]) in the aqueous solution was partitioned into the isolated LDs. Furthermore, silencing of CLO-encoding genes in the T. media cells led to a net decrease in the number and size of LDs. This coincided with a significant reduction in expression levels of TXS, DBAT and DBTNBT, key genes in the PTX biosynthesis pathway. Subsequently, the biosynthesis of PTX was declined in cell culture. In contrast, treatment of cells with 13-hydroperoxide C18:3, a substrate of the peroxygenase activity, induced the expression of CLOs, and, therefore, the accumulation of cellular LDs in the T. media cells cultures, thus increasing the PTX secretion. The accumulation of stable LDs is critically important for effective secretion of PTX. This is modulated by the expression of caleosins, a class of LD-associated proteins with a dual role conferring the structural stability of LDs as well as regulating lipidic bioactive metabolites via their enzymatic activity, thus enhancing the biosynthesis of PTX.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

PTX:

Paclitaxel

LDs:

Lipid droplets

CLO:

Caleosin

OLEO:

Oleosin

TCDD:

2,3,7,8-Polychlorinateddibenzo-p-dioxins

TAG:

Triacylglycerol

LOX:

Lipoxygenase

PXG:

Peroxygenase

JA:

Jasmonic acid

MeJA:

Methyl jasmonic acid

13-HPOT:

13-Hydroperoxide linolenic acid

13-LOX:

13-Lipoxygenase

AOS:

Allene oxide synthase

PXG:

Peroxygenase

DES:

Divinyl ether synthase

HPL:

Hydroperoxide lyase

References

  • Almagro L, Belchi-Navarro S, Martinez-Marquez A, Bru R, Pedreno MA (2015) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and coronatine. Plant Physiol Biochem 97:361–367

    Article  CAS  PubMed  Google Scholar 

  • Bachmann A, Hause B, Maucher H, Garbe E, Voros K, Weichert H, Wasternack C, Feussner I (2002) Jasmonate-induced lipid peroxidation in barley leaves initiated by distinct 13-LOX forms of chloroplasts. Biol Chem 383:1645–1657

    Article  CAS  PubMed  Google Scholar 

  • Bate NJ, Rothstein SJ (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J 16:561–569

    Article  CAS  PubMed  Google Scholar 

  • Belchi-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreno MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–89

    Article  CAS  PubMed  Google Scholar 

  • Besagni C, Kessler F (2013) A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237:463–470

    Article  CAS  PubMed  Google Scholar 

  • Bissery MC, Guenard D, Gueritte-Voegelein F, Lavelle F (1991) Experimental antitumor activity of taxotere (RP 56976, NSC 628503), a taxol analogue. Cancer Res 51:4845–4852

    CAS  PubMed  Google Scholar 

  • Bissett D, Kaye SB (1993) Taxol and taxotere—current status and future prospects. Eur J Cancer 29A:1228–1231

    Article  CAS  PubMed  Google Scholar 

  • Blee E (2002) Impact of phyto-oxylipins in plant defense. Trends Plant Sci 7:315–322

    Article  CAS  PubMed  Google Scholar 

  • Blee E, Durst F (1987) Hydroperoxide-dependent sulfoxidation catalyzed by soybean microsomes. Arch Biochem Biophys 254:43–52

    Article  CAS  PubMed  Google Scholar 

  • Blee E, Boachon B, Burcklen M, Le Guedard M, Hanano A, Heintz D, Ehlting J, Herrfurth C, Feussner I, Bessoule JJ (2014) The reductase activity of the Arabidopsis caleosin RESPONSIVE TO DESSICATION20 mediates gibberellin-dependent flowering time, abscisic acid sensitivity, and tolerance to oxidative stress. Plant Physiol 166:109–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonfill M, Palazón J, Cusidó RM, Joly S, Morales C, Piñol MT (2003) Influence of elicitors on taxane production and 3-hydroxy-3-methylglutaryl coenzymeA reductase activity in Taxus media cells. Plant Physiol Biochem 41:91–96

    Article  CAS  Google Scholar 

  • Boucher J, Cengelli F, Trumbic D, Marison IW (2008) Sorption of hydrophobic organic compounds (HOC) in rapeseed oil bodies. Chemosphere 70:1452–1458

    Article  CAS  PubMed  Google Scholar 

  • Boven E, Venema-Gaberscek E, Erkelens CA, Bissery MC, Pinedo HM (1993) Antitumor activity of taxotere (RP 56976, NSC 628503), a new taxol analog, in experimental ovarian cancer. Ann Oncol 4:321–324

    Article  CAS  PubMed  Google Scholar 

  • Braakhuis BJ, Hill BT, Dietel M, Kelland LR, Aapro MS, Zoli W, Lelieveld P (1994) In vitro antiproliferative activity of docetaxel (Taxotere), paclitaxel (Taxol) and cisplatin against human tumour and normal bone marrow cells. Anticancer Res 14:205–208

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cai Z, Kastell A, Knorr D, Smetanska I (2012) Exudation: an expanding technique for continuous production and release of secondary metabolites from plant cell suspension and hairy root cultures. Plant Cell Rep 31:461–477

    Article  CAS  PubMed  Google Scholar 

  • Chang W, Zhan GM, Zheng S, Li Y, Li X, Li W, Li G, Lin Z, Xie Z, Zhao Z, Lou H (2015) Trapping toxins within lipid droplets is a resistance mechanism in fungi. Nat Sci Rep 5:15133

    Article  CAS  Google Scholar 

  • Chapman KD, Dyer JM, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants: thematic review series: lipid droplet synthesis and metabolism: from yeast to man. J Lipid Res 53:215–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman KD, Aziz M, Dyer JM, Mullen RT (2019) Mechanisms of lipid droplet biogenesis. Biochem J 476:1929–1942

    Article  CAS  PubMed  Google Scholar 

  • Charuchinda P, Waditee-Sirisattha R, Kageyama H, Yamada D, Sirisattha S, Tanaka Y, Mahakhant A, Takabe T (2015) Caleosin from Chlorella vulgaris TISTR 8580 is salt-induced and heme-containing protein. Biosci Biotechnol Biochem 79:1119–1124

    Article  CAS  PubMed  Google Scholar 

  • Chen MC, Chyan CL, Lee TT, Huang SH, Tzen JT (2004) Constitution of stable artificial oil bodies with triacylglycerol, phospholipid, and caleosin. J Agric Food Chem 52:3982–3987

    Article  CAS  PubMed  Google Scholar 

  • Chiang CJ, Lin LJ, Chen CJ (2011) Caleosin-based nanoscale oil bodies for targeted delivery of hydrophobic anticancer drugs. J Nanopart Res 13:7127–7137

    Article  CAS  Google Scholar 

  • Chiang CJ, Lin SC, Lin LJ, Chen CJ, Chao YP (2012) Caleosin-assembled oil bodies as a potential delivery nanocarrier. Appl Microbiol Biotechnol 93:1905–1915

    Article  CAS  PubMed  Google Scholar 

  • Croteau R, Ketchum RE, Long RM, Kaspera R, Wildung MR (2006) Taxol biosynthesis and molecular genetics. Phytochem Rev 5:75–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crown J, O’Leary M, Ooi WS (2004) Docetaxel and paclitaxel in the treatment of breast cancer: a review of clinical experience. Oncologist 9(Suppl 2):24–32

    Article  CAS  PubMed  Google Scholar 

  • Cusido RM, Palazon J, Bonfill M, Navia-Osorio A, Morales C, Pinol MT (2002) Improved paclitaxel and baccatin III production in suspension cultures of Taxus media. Biotechnol Prog 18:418–423

    Article  CAS  PubMed  Google Scholar 

  • Cusido RM, Onrubia M, Sabater-Jara AB, Moyano E, Bonfill M, Goossens A, Angeles Pedreno M, Palazon J (2014) A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp. Biotechnol Adv 32:1157–1167

    Article  CAS  PubMed  Google Scholar 

  • De Vries J, Ischebeck T (2020) Ties between stress and lipid droplets pre-date seeds. Trends Plant Sci 25:1203–1214

    Article  PubMed  CAS  Google Scholar 

  • Deboever E, Deleu M, Mongrand S, Lins L, Fauconnier ML (2020) Plant-pathogen interactions: underestimated roles of phyto-oxylipins. Trends Plant Sci 25:22–34

    Article  CAS  PubMed  Google Scholar 

  • Esnay N, Dyer MJ, Mullen RT, Chapman KD (2020) Lipid droplet-peroxisome connections in plants. Contact 3:1–14

    Article  Google Scholar 

  • Exposito O, Syklowska-Baranek K, Moyano E, Onrubia M, Bonfill M, Palazon J, Cusido RM (2010) Metabolic responses of Taxus media transformed cell cultures to the addition of methyl jasmonate. Biotechnol Prog 26:1145–1153

    CAS  PubMed  Google Scholar 

  • Farag MA, Westphal H, Eissa TF, Wessjohann LA, Meyer A (2017) Effect of oxylipins, terpenoid precursors and wounding on soft corals’ secondary metabolism as analyzed via UPLC/MS and chemometrics. Molecules. https://doi.org/10.3390/molecules22122195

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Santos R, Izquierdo Y, Lopez A, Muniz L, Martinez M, Cascon T, Hamberg M, Castresana C (2020a) Protein profiles of lipid droplets during the hypersensitive defense response of Arabidopsis against Pseudomonas infection. Plant Cell Physiol 61:1144–1157

    Article  CAS  PubMed  Google Scholar 

  • Fett-Neto AG, Melanson SJ, Nicholson SA, Pennington JJ, Dicosmo F (1994a) Improved taxol yield by aromatic carboxylic acid and amino acid feeding to cell cultures of Taxus cuspidata. Biotechnol Bioeng 44:967–971

    Article  CAS  PubMed  Google Scholar 

  • Fett-Neto AG, Zhang WY, Dicosmo F (1994b) Kinetics of taxol production, growth, and nutrient uptake in cell suspensions of Taxus cuspidata. Biotechnol Bioeng 44:205–210

    Article  CAS  PubMed  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297

    Article  CAS  PubMed  Google Scholar 

  • Froissard M, D’Andrea S, Boulard C, Chardot T (2009) Heterologous expression of AtClo1, a plant oil body protein, induces lipid accumulation in yeast. FEMS Yeast Res 9:428–438

    Article  CAS  PubMed  Google Scholar 

  • Gao Q, Goodman JM (2015) The lipid droplet-a well-connected organelle. Front Cell Dev Biol 3:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Geem KR, Kim DH, Lee DW, Kwon Y, Lee J, Kim JH, Hwang I (2019) Jasmonic acid-inducible TSA1 facilitates ER body formation. Plant J 97:267–280

    Article  CAS  PubMed  Google Scholar 

  • Goossens A, Farmer EE (2019) Regulatory Oxylipins Anno 2019: Jasmonates Galore in the Plant Oxylipin Research Community. Plant Cell Physiol 60:2609–2612

    Article  CAS  PubMed  Google Scholar 

  • Grechkin AN (2002) Hydroperoxide lyase and divinyl ether synthase. Prostaglandins Other Lipid Mediat 68–69:457–470

    Article  PubMed  Google Scholar 

  • Griffiths G (2015) Biosynthesis and analysis of plant oxylipins. Free Radic Res 49:565–582

    Article  CAS  PubMed  Google Scholar 

  • Guenard D, Gueritte-Voegelein F, Dubois J, Potier P (1993) Structure-activity relationships of taxol and taxotere analogues. J Natl Cancer Inst Monogr 15:79–82

    Google Scholar 

  • Gueritte-Voegelein F, Guenard D, Potier P (1992) Anticancer substances of vegetable origin. spindle poisons: vincaleukoblastine, leurocristine and navelbine; taxol and taxotere. C R Seances Soc Biol Fil 186:433–440

    CAS  PubMed  Google Scholar 

  • Gueritte-Voegelein F, Guenard D, Dubois J, Wahl A, Potier P (1994) Chemical and biological studies on taxol (paclitaxel) and taxotere (docetaxel), new antineoplastic agents. J Pharm Belg 49:193–205

    CAS  PubMed  Google Scholar 

  • Gwak Y, Hwang YS, Wang B, Kim M, Jeong J, Lee CG, Hu Q, Han D, Jin E (2014) Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis. J Exp Bot 65:4317–4334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanano A, Burcklen M, Flenet M, Ivancich A, Louwagie M, Garin J, Blee E (2006) Plant seed peroxygenase is an original heme-oxygenase with an EF-hand calcium binding motif. J Biol Chem 281:33140–33151

    Article  CAS  PubMed  Google Scholar 

  • Hanano A, Almousally I, Shaban M, Blee E (2015a) A caleosin-like protein with peroxygenase activity mediates Aspergillus flavus development, aflatoxin accumulation, and seed infection. Appl Environ Microbiol 81:6129–6144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanano A, Almousally I, Shaban M, Moursel N, Shahadeh A, Alhajji E (2015b) Differential tissue accumulation of 2,3,7,8-tetrachlorinated dibenzo-p-dioxin in Arabidopsis thaliana affects plant chronology, lipid metabolism and seed yield. BMC Plant Biol 15:193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hanano A, Bessoule JJ, Heitz T, Blee E (2015c) Involvement of the caleosin/peroxygenase RD20 in the control of cell death during Arabidopsis responses to pathogens. Plant Signal Behav 10:e991574

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hanano A, Almousally I, Shaban M, Rahman F, Blee E, Murphy DJ (2016a) Biochemical, transcriptional, and bioinformatic analysis of lipid droplets from seeds of date palm (Phoenix dactylifera L.) and their use as potent sequestration agents against the toxic pollutant, 2,3,7,8-tetrachlorinated dibenzo-p-dioxin. Front Plant Sci 7:836

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanano A, Almousally I, Shaban M, Rahman F, Hassan M, Murphy DJ (2016b) Specific caleosin/peroxygenase and lipoxygenase activities are tissue-differentially expressed in date palm (Phoenix dactylifera L.) seedlings and are further induced following exposure to the toxin 2,3,7,8-tetrachlorodibenzo-p-dioxin. Front Plant Sci 7:2025

    PubMed  Google Scholar 

  • Hanano A, Alkara M, Almousally I, Shaban M, Rahman F, Hassan M, Murphy DJ (2018a) The peroxygenase activity of the Aspergillus flavus caleosin, AfPXG, modulates the biosynthesis of aflatoxins and their trafficking and extracellular secretion via lipid droplets. Front Microbiol 9:158

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanano A, Almousally I, Shaban M, Murphy DJ (2018b) Arabidopsis plants exposed to dioxin result in a WRINKLED seed phenotype due to 20S proteasomal degradation of WRI1. J Exp Bot 69:1781–1794

    Article  CAS  PubMed  Google Scholar 

  • Hanano A, Shaban M, Almousally I, Murphy DJ (2018c) Identification of a dioxin-responsive oxylipin signature in roots of date palm: involvement of a 9-hydroperoxide fatty acid reductase, caleosin/peroxygenase PdPXG2. Sci Rep 8:13181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hanano A, Almousally I, Shaban M (2019) Exposure of Aspergillus flavus NRRL 3357 to the environmental toxin, 2,3,7,8-tetrachlorinated dibenzo-p-dioxin, results in a hyper aflatoxicogenic phenotype: a possible role for caleosin/peroxygenase (AfPXG). Front Microbiol 10:2338

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanano A, Shaban M, Murphy DJ (2021) Functional involvement of caleosin/peroxygenase PdPXG4 in the accumulation of date palm leaf lipid droplets after exposure to dioxins. Environ Pollut 281:116966

    Article  CAS  PubMed  Google Scholar 

  • Hezari M, Ketchum RE, Gibson DM, Croteau R (1997) Taxol production and taxadiene synthase activity in Taxus canadensis cell suspension cultures. Arch Biochem Biophys 337:185–190

    Article  CAS  PubMed  Google Scholar 

  • Huang AHC (2018) Plant lipid droplets and their associated proteins: potential for rapid advances. Plant Physiol 176:1894–1918

    Article  PubMed  CAS  Google Scholar 

  • Hudak KA, Thompson JE (1996) Flotation of lipid-protein particles containing triacylglycerol and phospholipid from the cytosol of carnation petals. Physiol Plant 98:810–818

    Article  CAS  Google Scholar 

  • Hudak KA, Thompson JE (1997) Subcellular localization of secondary lipid metabolites including fragrance volatiles in carnation petals. Plant Physiol 114:705–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jamme F, Vindigni JD, Mechin V, Cherifi T, Chardot T, Froissard M (2013) Single cell synchrotron FT-IR microspectroscopy reveals a link between neutral lipid and storage carbohydrate fluxes in S. cerevisiae. PLoS ONE 8:e74421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang G, Yoon Y, Choi YD (2020b) Crosstalk with jasmonic acid integrates multiple responses in plant development. Int J Mol Sci. https://doi.org/10.3390/ijms21010305

    Article  PubMed  PubMed Central  Google Scholar 

  • Jennewein S, Croteau R (2001) Taxol: biosynthesis, molecular genetics, and biotechnological applications. Appl Microbiol Biotechnol 57:13–19

    Article  CAS  PubMed  Google Scholar 

  • Jolivet P, Roux E, D’Andrea S, Davanture M, Negroni L, Zivy M, Chardot T (2004) Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 42:501–509

    Article  CAS  PubMed  Google Scholar 

  • Kawahara M, Furuse K (1992) Recent results of anticancer drugs acting on microtubules—navelbine, taxol and taxotere for the treatment of lung cancer. Gan to Kagaku Ryoho 19:2150–2156

    CAS  PubMed  Google Scholar 

  • Kelland LR, Abel G (1992) Comparative in vitro cytotoxicity of taxol and taxotere against cisplatin-sensitive and -resistant human ovarian carcinoma cell lines. Cancer Chemother Pharmacol 30:444–450

    Article  CAS  PubMed  Google Scholar 

  • Koda Y (1992) The role of jasmonic acid and related compounds in the regulation of plant development. Int Rev Cytol 135:155–199

    Article  CAS  PubMed  Google Scholar 

  • Kory N, Farese RV Jr, Walther TC (2016) Targeting fat: mechanisms of protein localization to lipid droplets. Trends Cell Biol 26:535–546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684

    Article  CAS  PubMed  Google Scholar 

  • Lomova MV, Sukhorukov GB, Antipina MN (2010) Antioxidant coating of micronsize droplets for prevention of lipid peroxidation in oil-in-water emulsion. ACS Appl Mater Interfaces 2:3669–3676

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Xia W, Cao P, Xiao Z, Zhang Y, Liu M, Zhan C, Wang N (2019) Integrated transcriptome analysis reveals plant hormones jasmonic acid and salicylic acid coordinate growth and defense responses upon fungal infection in poplar. Biomolecules 9:12

    Article  PubMed Central  CAS  Google Scholar 

  • Ma P, Mumper JR (2013) Paclitaxel nano-delivery systems: a comprehensive review. J Nanomed Nanotechnol 4:1000164

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsuno R, Adachi S (1993) Lipid encapsulation technology—techniques and applications to food. Trends Food Sci Technol 4:256–261

    Article  CAS  Google Scholar 

  • Murphy DJ (1993) Structure, function and biogenesis of storage lipid bodies and oleosins in plants. Prog Lipid Res 32:247–280

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541–585

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ, Hernendez-Pinzon I, Patel K, Hope RG, McLauchlan J (2000) New insights into the mechanisms of lipid-body biogenesis in plants and other organisms. Front Microbiol 28:710–711

    CAS  Google Scholar 

  • Naested H, Frandsen GI, Jauh GY, Hernandez-Pinzon I, Nielsen HB, Murphy DJ, Rogers JC, Mundy J (2000) Caleosins: Ca2+-binding proteins associated with lipid bodies. Plant Mol Biol 44:463–476

    Article  CAS  PubMed  Google Scholar 

  • Navia-Osorio A, Garden H, Cusido RM, Palazon J, Alfermann AW, Pinol MT (2002) Production of paclitaxel and baccatin III in a 20-L airlift bioreactor by a cell suspension of Taxus wallichiana. Planta Med 68:336–340

    Article  CAS  PubMed  Google Scholar 

  • Nguyen LN, Nosanchuk JD (2011) Lipid droplet formation protects against gluco/lipotoxicity in Candida parapsilosis: an essential role of fatty acid desaturase Ole1. Cell Cycle 10:3159–3167

    Article  CAS  PubMed  Google Scholar 

  • Nixon M, Chan SHP (1997) A simple and sensitive colorimetric method for the determination of long-chain free fatty acids in subcellular organelles. Anal Biochem 97:403–409

    Article  Google Scholar 

  • Onrubia M, Cusido RM, Ramirez K, Hernandez-Vazquez L, Moyano E, Bonfill M, Palazon J (2013a) Bioprocessing of plant in vitro systems for the mass production of pharmaceutically important metabolites: paclitaxel and its derivatives. Curr Med Chem 20:880–891

    CAS  PubMed  Google Scholar 

  • Onrubia M, Moyano E, Bonfill M, Cusido RM, Goossens A, Palazon J (2013b) Coronatine, a more powerful elicitor for inducing taxane biosynthesis in Taxus media cell cultures than methyl jasmonate. J Plant Physiol 170:211–219

    Article  CAS  PubMed  Google Scholar 

  • Palazon J, Cusido RM, Bonfill M, Morales C, Pinol MT (2003) Inhibition of paclitaxel and baccatin III accumulation by mevinolin and fosmidomycin in suspension cultures of Taxus baccata. J Biotechnol 101:157–163

    Article  CAS  PubMed  Google Scholar 

  • Partridge M, Murphy DJ (2009) Roles of a membrane-bound caleosin and putative peroxygenase in biotic and abiotic stress responses in Arabidopsis. Plant Physiol Biochem 47:796–806

    Article  CAS  PubMed  Google Scholar 

  • Pasaribu B, Chen CS, Liao YK, Jiang PL, Tzen JTC (2017) Identification of caleosin and oleosin in oil bodies of pine pollen. Plant Physiol Biochem 111:20–29

    Article  CAS  PubMed  Google Scholar 

  • Pateraki I, Andersen-Ranberg J, Hamberger B, Maree Heskes A, Martens HJ, Zerbe P, Bach SS, Møller BL, Bohlmann J, Hamberger B (2014) Manoyl oxide (13R), the biosynthetic precursor of forskolin, is synthesized in specialized root cork cells in Coleus forskohlii. Plant Physiolgy 164:1222–1236

    Article  CAS  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyc M, Gidda SK, Seay D, Esnay N, Kretzschmar FK, Cai Y, Doner NM, Greer MS, Hull JJ, Coulon D, Brehelin C, Yurchenko O, de Vries J, Valerius O, Braus G, Ischebeck T, Chapman KD, Dyer JM, Mullen RT (2021) LDIP cooperates with SEIPIN and LDAP to facilitate lipid droplet biogenesis in Arabidopsis. Plant Cell 33:3076–3103

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahman F, Hassan M, Hanano A, Fitzpatrick DA, McCarthy CGP, Murphy DJ (2018a) Evolutionary, structural and functional analysis of the caleosin/peroxygenase gene family in the Fungi. BMC Genomics 19:976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman F, Hassan M, Rosli R, Almousally I, Hanano A, Murphy DJ (2018b) Evolutionary and genomic analysis of the caleosin/peroxygenase (CLO/PXG) gene/protein families in the Viridiplantae. PLoS ONE 13:e0196669

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramirez-Estrada K, Altabella T, Onrubia M, Moyano E, Notredame C, Osuna L, Vanden Bossche R, Goossens A, Cusido RM, Palazon J (2016) Transcript profiling of jasmonate-elicited Taxus cells reveals a beta-phenylalanine-CoA ligase. Plant Biotechnol J 14:85–96

    Article  CAS  PubMed  Google Scholar 

  • Rangel C, Niell H, Miller A, Cox C (1994) Taxol and taxotere in bladder cancer: in vitro activity and urine stability. Cancer Chemother Pharmacol 33:460–464

    Article  CAS  PubMed  Google Scholar 

  • Reinbothe C, Springer A, Samol I, Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 276:4666–4681

    Article  CAS  PubMed  Google Scholar 

  • Ringel I, Horwitz SB (1991) Studies with RP 56976 (taxotere): a semisynthetic analogue of taxol. J Natl Cancer Inst 83:288–291

    Article  CAS  PubMed  Google Scholar 

  • Romani F, Banić E, Florent NS, Kanazawa T, Goodger QDJ, Mentink AR, Dierschke T, Zachgo S, Ueda T, Bowman LJ, Tsiantis M, Moreno JE (2020) Oil body formation in Marchantia polymorpha is controlled by MpC1HDZ and serves as a defense against arthropod herbivores. Curr Biol 30:2815–2828

    Article  CAS  PubMed  Google Scholar 

  • Sabater-Jara AB, Onrubia M, Moyano E, Bonfill M, Palazon J, Pedreno MA, Cusido RM (2014) Synergistic effect of cyclodextrins and methyl jasmonate on taxane production in Taxus x media cell cultures. Plant Biotechnol J 12:1075–1084

    Article  CAS  PubMed  Google Scholar 

  • Sarmiento C, Ross JHE, Herman E, Murphy DJ (1997) Expression and subcellular targeting of a soybean oleosin in transgenic rapeseed. Implications for the mechanism of oil-body formation in seeds. Plant J 11:783–796

    Article  CAS  PubMed  Google Scholar 

  • Savchenko TV, Zastrijnaja OM, Klimov VV (2014) Oxylipins and plant abiotic stress resistance. Biochem Mosc 79:362–375

    Article  CAS  Google Scholar 

  • Shao F, Wilson IW, Qiu D (2021) The research progress of taxol in Taxus. Curr Pharm Biotechnol 22:360–366

    Article  CAS  PubMed  Google Scholar 

  • Sharma VK, Monostori T, Gobel C, Hansch R, Bittner F, Wasternack C, Feussner I, Mendel RR, Hause B, Schulze J (2006) Transgenic barley plants overexpressing a 13-lipoxygenase to modify oxylipin signature. Phytochemistry 67:264–276

    Article  CAS  PubMed  Google Scholar 

  • Shimada TL, Hara-Nishimura I (2015) Leaf oil bodies are subcellular factories producing antifungal oxylipins. Curr Opin Plant Biol 25:145–150

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan V, Pestchanker L, Moser S, Hirasuna TJ, Taticek RA, Shuler ML (1995) Taxol production in bioreactors: kinetics of biomass accumulation, nutrient uptake, and taxol production by cell suspensions of Taxus baccata. Biotechnol Bioeng 47:666–676

    Article  CAS  PubMed  Google Scholar 

  • Stage TB, Bergmann TK, Kroetz DL (2018) Clinical pharmacokinetics of paclitaxel monotherapy: an updated literature review. Clin Pharmacokinet 57:7–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98:12837–12842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talebi M, Ghassempour A, Talebpour Z, Rassouli A, Dolatyari L (2004) Optimization of the extraction of paclitaxel from Taxus baccata L. by the use of microwave energy. J Sep Sci 27:1130–1136

    Article  CAS  PubMed  Google Scholar 

  • Tanchak MA, Fowke LC (1987) The morphology of multivesicular bodies in soybean protoplasts and their role in endocytosis. Protoplasma 138:173–182

    Article  Google Scholar 

  • Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzen JT, Huang AH (1992) Surface structure and properties of plant seed oil bodies. J Cell Biol 117:327–335

    Article  CAS  PubMed  Google Scholar 

  • Tzen JTC, Lie GC, Huang AHC (1992) Characterization of the charged components and their topology on the surface of plant seed oil bodies. J Biol Chem 267:15626–15634

    Article  CAS  PubMed  Google Scholar 

  • Tzen J, Cao Y, Laurent P, Ratnayake C, Huang A (1993) Lipids, proteins, and structure of seed oil bodies from diverse species. Plant Physiol 101:267–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Herpen NA, Schrauwen-Hinderling VB (2008) Lipid accumulation in non-adipose tissue and lipotoxicity. Physiol Behav 94:231–241

    Article  PubMed  CAS  Google Scholar 

  • Vongpaseuth K, Roberts SR (2007) Advancements in the understanding of paclitaxel metabolism in tissue culture. Curr Pharm Biotechnol 8:219–236

    Article  CAS  PubMed  Google Scholar 

  • Wani MC, Horwitz SB (2014) Nature as a remarkable chemist: a personal story of the discovery and development of taxol. Anticancer Drugs 25:482–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whisson SC, Avrova AO, Van West P, Jones JT (2005) A method for double-stranded RNA-mediated transient gene silencing in Phytophthora infestans. Mol Plant Pathol 6:153–163

    Article  CAS  PubMed  Google Scholar 

  • White DA, Fisk ID, Gray DA (2006) Characterisation of oat (Avena sativa L.) oil bodies and intrinsically associated E-vitamers. J Cereal Sci 43:244–249

    Article  CAS  Google Scholar 

  • Willmann MR (2002) Plant defense in the absence of jasmonic acid. Trends Plant Sci 7:8–9

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Lin L (2003) Enhancement of taxol production and release in Taxus chinensis cell cultures by ultrasound, methyl jasmonate and in situ solvent extraction. Appl Microbiol Biotechnol 62:151–155

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Qu Y, Lian Y, Chapman M, Chapman N, Xin J, Xin H, Liu L (2020) A new insight into the mechanism for cytosolic lipid droplet degradation in senescent leaves. Physiol Plant 168:835–844

    Article  CAS  PubMed  Google Scholar 

  • Zhi Y, Taylor MC, Campbell PM, Warden AC, Shrestha P, El Tahchy A, Rolland V, Vanhercke T, Petrie JR, White RG, Chen W, Singh SP, Liu Q (2017) Comparative lipidomics and proteomics of lipid droplets in the mesocarp and seed tissues of Chinese tallow (Triadica sebifera). Front Plant Sci 8:1339

    Article  PubMed  PubMed Central  Google Scholar 

  • Zienkiewicz K, Zienkiewicz A (2020c) Degradation of lipid droplets in plants and algae—right time, many paths, one goal. Front Plant Sci 11:579019

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Prof. Dr. Ibrahim OTHMAN, Director General of the Atomic Energy Commission of Syria and Dr. Nizar MIRALI, Head of the Department of Molecular Biology and Biotechnology for their crucial support. Our co-authors, Rosa M. Cusido and Edgar Perez-Matas, also thank the Spanish MEIC (BIO2017-82374-R) (AEI/FEDER, UE) and the Generalitat de Catalunya (2017SGR242).

Funding

No funding to be declared.

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Biotechnology, Atomic Energy Commission of Syria (AECS), P.O. Box 6091, Damascus, Syria

    Abdulsamie Hanano & Mouhnad Shaban

  2. Secció de Fisiologia Vegetal, Facultat de Farmacia, Universitat de Barcelona, Av. Joan XXIII Sn., 08028, Barcelona, Spain

    Edgar Perez-Matas & Rosa M. Cusido

  3. Genomics and Computational Biology Group, University of South Wales, Pontypridd, Wales, UK

    Denis J. Murphy

Authors
  1. Abdulsamie Hanano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edgar Perez-Matas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mouhnad Shaban
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosa M. Cusido
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Denis J. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AH conceived and designed the experimental work and wrote the first draft of manuscript. EPM contributed to knowledge transfer of tissues culture protocols. MS performed the experiments. RMC supervised the work, read and commented the manuscript. DJM revised and edited the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Abdulsamie Hanano.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Availability of data and materials

Not applicable.

Code availability

Not applicable.

Ethics approval

Not applicable.

Consent to participate and consent for publication

All of the authors contributed substantially to the manuscript and approved the final submission in Plant Cell Reports.

Additional information

Communicated by Kunpeng Jia.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 39 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hanano, A., Perez-Matas, E., Shaban, M. et al. Characterization of lipid droplets from a Taxus media cell suspension and their potential involvement in trafficking and secretion of paclitaxel. Plant Cell Rep 41, 853–871 (2022). https://doi.org/10.1007/s00299-021-02823-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-021-02823-0

Keywords

Search

Navigation