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

Industrial Crops and Products

Volumn 122, Issue , 2018, Pages 732-739

  Sitarek, Przemysław ^a   Kowalczyk, Tomasz ^b   Picot, Laurent ^c   Michalska Hejduk, Dorota ^b   Bijak, Michał ^b   Białas, Adam J ^a   Wielanek, Marzena ^b   Śliwiński, Tomasz ^b   Skała, Ewa ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b UNIVERSITY OF LODZ   (Poland)

^c French National Centre for Scientific Research   (France)

Author keywords

Antioxidant activity; Antiproliferative effect; AtPAP1transgenic roots of Leonurus sibiricus; Bioreactor; C4H and 4CL genes expression; PAL

Indexed keywords

ANTIOXIDANTS; BIOACTIVITY; BIOCONVERSION; BLOOD; CHLORINE COMPOUNDS; CROPS; ORGANIC ACIDS; PLANTS (BOTANY);

ACID PRODUCTION; ANTIOXIDANT ACTIVITIES; ANTIPROLIFERATIVE EFFECT; ATPAP1TRANSGENIC ROOT OF LEONURI SIBIRICU; C4H AND 4CL GENE EXPRESSION; GENES EXPRESSION; PAL; PHENOLIC ACIDS; TRANSCRIPTIONAL FACTORS; TRANSGENIC ROOTS;

BIOREACTORS;

ANTIOXIDANT; BIOACTIVITY; BIOLOGICAL PRODUCTION; BIOMASS; BIOREACTOR; GENE EXPRESSION; GENETIC ANALYSIS; GROWTH; HERB; PHENOLIC COMPOUND; TRANSGENIC PLANT;

LEONURUS SIBIRICUS;

EID: 85050284116     PISSN: 09266690     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.indcrop.2018.06.059     Document Type: Article

References (37)

1. Anh Tuan, P., Yeon Kwon, D., Lee, S., Arasu, M.F., Al-Dhabi, N.A., Park, N.I., Park, S.U., Enhancement of chlorogenic acid production in hairy roots of Platycodon grandiflorum by over-expression of an Arabidopsis thaliana transcription factor AtPAP1. Int. J. Mol. Sci. 15:8 (2014), 14743–14752.
2. Atanasov, A.G., Waltenberger, B., Pferschy-Wenzig, E.A., Linder, T., Wawrosch, C., Uhrin, P., Temml, V., Wang, L., Schwaiger, S., Heiss, E.H., Rollinger, J.M., Schuster, D., Breuss, J.M., Bochkov, V., Mihovilovic, M.D., Bauer, R., Dirsch, V.M., Stuppner, H., Discovery and resupply of pharmacologically active plant-derived natural products: a review. Biotechnol. Adv. 33:8 (2015), 1582–1614.
3. Banerjee, S., Singh, S., Ur Rahman, L., Biotransformation studies using hairy root cultures – a review. Biotechnol. Adv. 30:3 (2012), 461–468, 10.1016/j.biotechadv.2011.08.010.
4. Baque, A., Sang-Hyun, M., Lee, E.J., Zhong, J.J., Paek, K.-Y., Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants using bioreactor. Biotechnol. Adv. 30 (2012), 1255–1267.
5. Chattopadhyay, S., Srivastava, A.K., Bhojwani, S.S., Bisaria, V.S., Production of podophyllotoxin by plant cell cultures of Podophyllum hexandrum in bioreactor. J. Biosci. Bioeng. 93:2 (2002), 215–220.
6. Chmiel, A., Ledakowicz, S., Pawlowska, B., The mist bioreactor for cultures of transformed roots. 28th Conference SSCHE, Proceedings on CD ROM, May 21–25, Tatranske Matliare (SK), 2001.
7. Dadé M.M., Schinella, G.R., Fioravanti, D.E., Alfiotournier, H., Antioxidant and cytotoxic properties of an aqueous extract from the Argentinean plant Hedeoma multiflorum. Pharm. Biol. 49:6 (2011), 633–639, 10.3109/13880209.2010.526949.
8. de Freitas, M.M., Ribeiro Fontes, P., Monteiro Souza, P., Fagg, C.W., Neves Silva Guerra, E., de Medeiros Nóbrega, Y.K., Silveira, D., Fonseca-Bazzo, Y., Simeoni, L.A., Homem-de-Mello, M., Oliveira Magalhães, P., Extracts of Morus nigra L. leaves standardized in chlorogenic acid, rutin and isoquercitrin: tyrosinase inhibition and cytotoxicity. PLoS One, 11(9), 2016, e0163130.
9. deOliveira Melo, M.N., Passos Oliveira, A., Wiecikowski, A.F., Sampaio Carvalho, R., de Lima Castro, J., Alves Gomesde Oliveira, F., Marcelo Gualberto Pereira, H., Feoda Veiga, V., Marques Alves Capella, M., Rocha, L., Holandino, C., Phenolic compounds from Viscum album tinctures enhanced antitumor activity in melanoma murine cancer cells. Saudi Pharm. J. 26:3 (2018), 311–322.
10. Du, M., Wu, X.J., Ding, J., Hu, Z.B., White, K.N., Branford-White, C.J., Astragaloside IV and polysaccharide production by hairy roots of Astragalus membranaceus in bioreactors. Biotechnol. Lett. 25 (2003), 1853–1856.
11. Farah, A., Monteiro, M., Donangelo, C.M., Lafay, S., Chlorogenic acids from green coffee extract are highly bioavailable in humans. J. Nutr. 138 (2008), 2309–2315.
12. Janaszewska, A., Bartosz, G., Assay of total antioxidant capacity: comparison of four methods as applied to human blood plasma. Scand. J. Clin. Lab Invest. 62 (2002), 231–236.
13. Kolodziejczyk-Czepas, J., Nowak, P., Moniuszko-Szajwaj, B., Kowalska, I., Stochmal, A., Free radical scavenging actions of three Trifolium species in the protection of blood plasma antioxidant capacity in vitro. Pharm. Biol., 2015, 1–8, 10.3109/13880209.2014.974064.
14. Kolodziejczyk-Czepas, J., Bijak, M., Saluk, J., Ponczek, M.B., Zbikowska, H.M., Nowak, P., Tsirigotis-Maniecka, M., Pawlaczyk, I., Radical scavenging and antioxidant effects of Matricaria chamomilla polyphenolic-polysaccharide conjugates. Int. J. Biol. Macromol. 72 (2015), 1152–1158, 10.1016/j.ijbiomac.2014.09.032.
15. Kusakari, K., Yokoyama, M., Inomata, M., Gozu, Y., Katagiri, C., Sugimoto, Y., Large-scale production of saikosaponins through root culturing of Bupleurum falcatum L. using modified airlift reactors. J. Biosci. Bioeng. 113:1 (2012), 99–105.
16. Kuźma, Ł., Kaiser, M., Wysokińska, H., The production and antiprotozoal activity of abietane diterpenes in Salvia austriaca hairy roots grown in shake flasks and bioreactor. Prep. Biochem. Biotechnol. 47:1 (2017), 58–66, 10.1080/10826068.2016.1168745.
17. Li, H.-R., Habasi, M., Xie, L.-Z., Ais, H.-A., Effect of chlorogenic acid on melanogenesis of B16 melanoma cells. Molecules 19 (2014), 12940–12948, 10.3390/molecules190912940.
18. Luo, J., Butelli, E., Hill, L., Parr, A., Niggeweg, R., Bailey, P., Weisshaar, B., Martin, C., AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J. 56 (2008), 316–326.
19. Oliveira, A.S., Cercato, L.M., de Santana Souza, M.T., Melo, A.J.O., Lima, B.D.S., Duarte, M.C., Araujo, A.A.S., de Oliveira E Silva, A.M., Camargo, E.A., The ethanol extract of Leonurus sibiricus L. induces antioxidant, antinociceptive and topical anti-inflammatory effects. J. Ethnopharmacol. 206 (2017), 144–151, 10.1016/j.jep.2017.05.029.
20. Qiu, J., Sun, S., Luo, S., et al. Arabidopsis AtPAP1 transcription factor induces anthocyanin production in transgenic Taraxacum brevicorniculatum. Plant Cell Rep., 33, 2014, 669, 10.1007/s00299-014-1585-8.
21. Raghavendrarao, S., Anil Kumar, M., Ranjitha, K., Bollipo, D., A review on advanced methods in plant gene targeting. JGEB 15:2 (2017), 317–321.
22. Re, R., Pellegrini, N., Proteggente, A., et al. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 26 (1999), 1231–1237.
23. Rivera, A.L., Gómez-Lim, M., Fernández, F., Loske, A.M., Physical methods for genetic plant transformation. Phys. Life Rev. 9 (2012), 308–345.
24. Sayed, A., Alam, A., Islam, S., Ali, T., Ullah, E., Zaffar Shibly, A., Ali, A., Hasan-Olive, M., Leonurus sibiricus L. (honeyweed): a review of its phytochemistry and pharmacology. Asian Pac. J. Trop. Biomed. 6:12 (2016), 1076–1080.
25. Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3 (2008), 1101–1108.
26. Shahidi, F., Chandrasekara, A., Hydroxycinnamates and their in vitro and in vivo antioxidant activities. Phytochem. Rev. 9 (2010), 147–170.
27. Sitarek, P., Skała, E., Toma, M., Wielanek, M., Szemraj, J., Nieborowska-Skorska, M., Kolasa, M., Skorski, T., Wysokińska, H., Śliwiński, T., 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. 37:7 (2016), 8753–8764, 10.1007/s13277-015-4714-2.
28. Sitarek, P., Skała, E., Wysokińska, H., Wielanek, M., Szemraj, J., Toma, M., Śliwiński, T., The effect of Leonurus sibiricus plant extracts on stimulating repair and protective activity against oxidative DNA damage in CHO cells and content of phenolic compounds. Oxid. Med. Cell Longev., 2016, 2016, 5738193, 10.1155/2016/5738193.
29. Sitarek, P., Rijo, P., Garcia, C., Skała, E., Kalemba, D., Białas, A.J., Szemraj, J., Pytel, D., Toma, M., Wysokińska, H., Śliwiński, T., Antibacterial, anti-inflammatory, antioxidant, and antiproliferative properties of essential oils from hairy and Normal roots of Leonurus sibiricus L. and their chemical composition. Oxid. Med. Cell Longev., 2017, 2017, 7384061, 10.1155/2017/7384061.
30. Sitarek, P., Skała, E., Toma, M., Wielanek, M., Szemraj, J., Skorski, T., Białas, A.J., Sakowicz, T., Kowalczyk, T., Radek, M., Wysokińska, H., Śliwiński, T., Transformed root extract of Leonurus sibiricus induces apoptosis through intrinsic and extrinsic pathways in various grades of human glioma cells. Pathol. Oncol. Res. 23:3 (2017), 679–687, 10.1007/s12253-016-0170-6.
31. Sitarek, P., Kowalczyk, T., Rijo, P., Białas, A.J., Wielanek, M., Wysokińska, H., Garcia, C., Toma, M., Śliwiński, T., Skała, E., Over-expression of AtPAP1 transcriptional factor enhances phenolic acid production in transgenic roots of Leonurus sibiricus L. and their biological activities. Mol. Biotechnol. 60:1 (2018), 74–82, 10.1007/s12033-017-0048-1.
32. Sivakumar, G., Bioreactor technology: a novel industrial tool for high-tech production of bioactive molecules and biopharmaceuticals from plant roots. Biotechnol. J. 1 (2006), 1419–1427, 10.1002/biot.200600117.
33. Skała, E., Kicel, A., Olszewska, M.A., Kiss, A.K., Wysokińska, H., Establishment of hairy root cultures of Rhaponticum carthamoides (Willd.) Iljin for the production of biomass and caffeic acid derivatives. BioMed. Res. Int. 181098 (2015), 1–11.
34. Srivastava, S., Srivastava, A.K., Hairy root culture for mass-production of high-value secondary metabolites. Crit. Rev. Biotechnol. 27:1 (2007), 29–43.
35. Verma, P.C., Singh, H., Negi, A.S., Saxena, G., Rahman, L., Banerjee, S., Yield enhancement strategies for the production of picroliv from hairy root culture of Picrorhiza kurroa Royle ex Benth. Plant Signal. Behav., 10(5), 2015, 10.1080/15592324.2015.1023976.
36. Wu, C.H., Murthy, H.N., Hah, 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. 29 (2007), 1179–1182, 10.1007/s10529-007-9399-1.
37. Zhang, Y., Yan, Y.P., Wang, Z.Z., The Arabidopsis PAP1 transcription factor plays an important role in the enrichment of phenolic acids in Salvia miltiorrhiza. J. Agric. Food Chem. 58 (2010), 12168–12175.