Advertisement

Chemical Papers

, Volume 71, Issue 6, pp 1091–1106 | Cite as

Production of camptothecin in the elicited callus cultures of Nothapodytes nimmoniana (J. Graham) Mabberly

  • Tasiu IsahEmail author
Original Paper

Abstract

The biotechnological approach of in vitro cultures elicitation offers an alternative strategy for the production of camptothecin (CPT) in Nothapodytes nimmoniana to mitigate indiscriminate harvest of the endangered natural population for the alkaloid. Yeast extract (YE) and vanadyl sulfate (VS) elicitors were used to enhance the biosynthesis of CPT in hypocotyl-derived callus cultures of N. nimmoniana by cultivation using solid and liquid Murashige and Skoog (MS) medium amended with NAA + BAP (2.0 + 1.0 mg L−1). Effects of the two elicitors on biomass and CPT production at 6.25, 12.5, 25, 50 and 75 mg L−1 concentrations using callus cultures from three cell lines were evaluated after 15, 30 and 45 days culture. Yeast extract elicitor treatments showed a linear enhancement effect on biomass and CPT production up to 50 mg L−1 YE and beyond the concentrations, no significant effect was observed. Enhanced biomass and CPT production were achieved with VS elicitor up to 25 mg L−1 concentrations but, 50 and 75 mg L−1 VS had minimal effects on biomass and CPT production in callus sources and incubation duration-dependent manner. The intracellular yield of CPT in liquid media-cultivated cultures at concentrations of the two elicitors was lower when compared to solid media treatments relative control due to the extracellular accumulation but, higher overall production. Accumulation of the biomass showed association with produced CPT in the elicitor treatments and control cultures.

Keywords

Camptothecin Elicitation Yeast extract Vanadyl sulfate Nothapodytes nimmoniana Chromatography 

Notes

Acknowledgements

This work was financially supported by the agreed terms between Department of Biotechnology, Government of India New Delhi and The World Academy of Sciences for the Advancement of Science in Developing Countries (TWAS) Trieste Italy, through DBT–TWAS Postgraduate Research Fellowship. I am highly grateful to Hamdard University New Delhi, India for providing research facilities.

Supplementary material

11696_2016_56_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)

References

  1. Abraham F, Bhatt A, Keng CL, Indrayanto G, Sulaiman SF (2011) Effect of yeast extract and chitosan on shoot proliferation, morphology and antioxidant activity of Curcuma mangga in vitro plantlets. Afr J Biotechnol 10(40):7787–7795. doi: 10.5897/AJB10.1261 CrossRefGoogle Scholar
  2. Bhagwath SG, Hjortso MA (2000) Statistical analysis of elicitation strategies for thiarubrine A production in hairy root cultures of Ambrosia artemisiifolia. J Biotechnol 80(2):159–167. doi: 10.1016/S0168-1656(00)00256-X CrossRefGoogle Scholar
  3. Boller T (1995) Chemo-perception of microbial signals in plant cells. Ann Rev Plant Physiol Plant Mol Biol 46:189–214. doi: 10.1146/annurev.pp.46.060195.001201 CrossRefGoogle Scholar
  4. Bonfill M, Palazon J, Cusido RM et al (2003) Influence of elicitors on taxane production and 3-hydroxy-3-methyl-glutaryl coenzyme A reductase activity in the Taxus media cells. Plant Physiol 108:1171–1178. doi: 10.1016/S0981-9428(02)00013-X Google Scholar
  5. Chen H, Chen F (2000) Effects of yeast elicitor on the growth and secondary metabolism of a high-tanshinone-producing line of the Ti-transformed Salvia miltiorrhiza cells in suspension culture. Process Biochem 35(8):837–840. doi: 10.1016/S0032-9592(99)00146-6 CrossRefGoogle Scholar
  6. Chuntaratin P (2006) Production of plumbagin by hairy root, callus, and cell suspension cultures of Plumbago indica L. A Thesis submitted to graduate school, Kasetsart University, ISBN 974-16-2187-6, pp 97Google Scholar
  7. Ciddi V, Shuler ML (2000) Camptothecin from callus cultures of Nothapodytes foetida. Biotechnol Lett 22(2):129–132. doi: 10.1023/A:1005666223003 CrossRefGoogle Scholar
  8. Clements MK, Jone CB, Cumming M, Daud SS (1999) Antiangiogenic potential of camptothecin and topotecan. Cancer Chemother Pharmacol 44:411–416. doi: 10.1007/s002800050997 CrossRefGoogle Scholar
  9. Dandin VS, Murthy HN (2012) Enhanced in vitro multiplication of Nothapodytes nimmoniana Graham using semi-solid and liquid cultures and estimation of camptothecin in the regenerated plants. Acta Physiol Plant 34:1381–1386. doi: 10.1007/s11738-012-0934-x CrossRefGoogle Scholar
  10. Fulzele DP, Satdive RK (2005) Comparison of techniques for the extraction of the anti-cancer drug camptothecin from Nothapodytes foetida. J Chromatogr Anal 1063(2):9–13. doi: 10.1016/j.chroma.2004.11.020 CrossRefGoogle Scholar
  11. Fulzele DP, Satdive RK, Pol BB (2001) Growth and production of camptothecin by cell suspension cultures of Nothapodytes foetida. Planta Med 67(2):150–152. doi: 10.1055/s-2001-11519 CrossRefGoogle Scholar
  12. Furmanowa M, Olędzka H, Sykłowska-Baranek K et al (2000) Increased taxane accumulation in callus cultures of Taxus cuspidata and Taxus × media by some elicitors and precursors. Biotechnol Lett 22(18):1449–1452. doi: 10.1023/A:1005611114628 CrossRefGoogle Scholar
  13. Govindachari TR, Viswanathan N (1972) Alkaloids of Mappia foetida. Phytochem 11(12):3529. doi: 10.1016/S0031-9422(00)89852-0 CrossRefGoogle Scholar
  14. Hahn MG, Albersheim P (1978) Host–pathogen interactions. Plant Physiol 62:107–111. doi: 10.1104/pp.68.5.1161 CrossRefGoogle Scholar
  15. Hakkim FL, Kalyani S, Essa M et al (2011) Production of rosmarinic in Ocimum sanctum cell cultures by the influence of sucrose, phenylalanine, yeast extract, and methyl jasmonate. Int J Biol Med Res 2:1070–1074Google Scholar
  16. Holden MA, Holden PR, Yeoman MM (1988) Elicitation of cell cultures. Manipulating secondary metabolism in culture. Cambridge University Press, Cambridge, pp 57–65Google Scholar
  17. Hong MLK, Bhatt A, Ping NS, Keng CL (2012) Detection of elicitation effect on Hyoscyamus niger L. root cultures for the root growth and production of tropane alkaloids. Romanian Biotechnol Lett 17(3):7341Google Scholar
  18. Hussain MS, Fareed S, Ansari S et al (2012) Current approaches toward the production of plant secondary metabolites. J Pharm BioAllied Sci 4:10–20. doi: 10.4103/0975-7406.92725 CrossRefGoogle Scholar
  19. Isah T (2016) Induction of somatic embryogenesis in woody plants. Acta Physiol Plant 38:118. doi: 10.1007/s11738-016-2134-6 CrossRefGoogle Scholar
  20. Isah T, Mujib A (2015a) In vitro propagation and camptothecin production in Nothapodytes nimmoniana. Plant Cell Tiss Organ Cult 121:1–10. doi: 10.1007/s11240-014-0683-1 CrossRefGoogle Scholar
  21. Isah T, Mujib A (2015b) Camptothecin from Nothapodytes nimmoniana: review on biotechnology applications. Acta Physiol Plant 37:106. doi: 10.1007/s11738-015-1854-3 CrossRefGoogle Scholar
  22. Isah T, Mujib A (2015c) Enhanced in vitro seedling recovery in Nothapodytes nimmoniana. Brit Biotechnol J 6(1):2231–2927. doi: 10.9734/bbj/2015/15368 CrossRefGoogle Scholar
  23. Jaisi A, Panichayupakaranant P (2016) Increased production of plumbagin in Plumbago indica root cultures by biotic and abiotic elicitors. Biotechnol Lett 38:351–355. doi: 10.1007/s10529-015-1969-z CrossRefGoogle Scholar
  24. Jartoodeh SV, Davarynejad GH, Tehranifar A, Kaveh H, Bisheh HA (2013) Reducing browning problem in micropropagation of three pear cultivars; Sebri, Shekari and Natanz. Curr Opin Agric 2(1):25Google Scholar
  25. Jisha KG (2006) A study on the production of camptothecin from Ophiorrhiza mungos and Nothapodytes foetida using cell and tissue culture. Thesis submitted to Mahatma Gandhi Univ. Through Amala Cancer Res Centre, Thrissur, in partial fulfillment of the requirements for the award of Doctor of PhilosophyGoogle Scholar
  26. Kai G, Wu C, Gen L et al (2015) Biosynthesis and biotechnological production of anti-cancer drug camptothecin. Phytochem Rev 14(3):525–539. doi: 10.1007/s11101-015-9405-5 CrossRefGoogle Scholar
  27. Kargi F, Potts P (1991) Effect of various stress factors on indole alkaloid formation by Catharanthus roseus (periwinkle) cells. Enzyme Microb Technol 13(9):760–763. doi: 10.1016/0141-0229(91)90056-G CrossRefGoogle Scholar
  28. Karwasara VS, Dixit VK (2013) Culture medium optimization for camptothecin production in cell suspension cultures of Nothapodytes nimmoniana (J. Grah.) Mabb. Plant Biotechnol Rep 12:1–13. doi: 10.1007/s11816-012-0270-z Google Scholar
  29. Kedari P, Malpathak N (2013) Subcellular localization and quantification of camptothecin in different plant parts of Chonemorpha fragrans. Adv Zool Bot 1:34–38. doi: 10.13189/azb.2013.010203 Google Scholar
  30. Kulkarni AV, Patwardhan AA, Lele U, Malpathak NP (2010) Production of camptothecin in cultures of Chonemorpha grandiflora. Pharmacogn Res 2(5):296–299. doi: 10.4103/0974-8490.72327 CrossRefGoogle Scholar
  31. Kümmritz S, Louis M, Haas C et al (2016) Fungal elicitors combined with a sucrose feed significantly enhance triterpene production of a Salvia fruticosa cell suspension. Appl Microbiol Biotechnol 100(16):7071–7082. doi: 10.1007/s00253-016-7432-9 CrossRefGoogle Scholar
  32. Lee-Parsons CW, Ertürk S, Tengtrakool J (2004) Enhancement of ajmalicine production in Catharanthus roseus cell cultures with methyl jasmonate is dependent on timing and dosage of elicitation. Biotechnol Lett 26(20):1595–1599. doi: 10.1023/B:BILE.0000045825.37395.94 CrossRefGoogle Scholar
  33. Li S, Zhang W, Nothrup K, Zhang D (2014) Distribution of the Camptotheca decaisne: an endangered status. Pharma Crops 5:135–139. doi: 10.2174/2210290601405010135 CrossRefGoogle Scholar
  34. Lindsey K (1985) Manipulation by the nutrient limitation of the biosynthetic activity of immobilized cells of Capsicum frutescens Mill. ev. annuum. Planta 165:126–133. doi: 10.1007/BF00392221 CrossRefGoogle Scholar
  35. Liu YQ, Li WQ, Morris-Natschke SL et al (2015) Perspectives on biologically active camptothecin derivatives. Med Res Rev 35:753–789. doi: 10.1002/med.21342 CrossRefGoogle Scholar
  36. Loc N, Giang N (2012) Effects of elicitors on the enhancement of asiaticoside biosynthesis in cell cultures of centella (Centella asiatica L. Urban). Chem Pap 66(7):642–648. doi: 10.2478/s11696-012-0168-9 CrossRefGoogle Scholar
  37. Loc NH, Anh NHT, Khuyen LTM et al (2014) Effects of yeast extract and methyl jasmonate on the enhancement of solasodine biosynthesis in cell cultures of Solanum hainanense Hance. J BioSci Biotechnol 3(1):1–6Google Scholar
  38. Malik SS, Laura JS (2014) Distribution of camptothecin through the plant kingdom. Int J Curr Res 6(5):6497–6507Google Scholar
  39. Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 26:548–560. doi: 10.1016/j.biotechadv.2008.07.001 CrossRefGoogle Scholar
  40. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  41. Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tiss Organ Cult 118(1):1–16. doi: 10.1007/s11240-014-0467-7 CrossRefGoogle Scholar
  42. Onrubia M, Moyano E, Bonfill M et al (2010) An approach to the molecular mechanism of methyl jasmonate and vanadyl sulfate elicitation in Taxus baccata cell cultures: the role of txs and bapt gene expression. Biochem Eng J 53(1):104–111. doi: 10.1016/j.bej.2010.10.001 CrossRefGoogle Scholar
  43. Palazon J, Cusido RM, Bonfill M et al (2003) Elicitation of different Panax ginseng transformed root phenotypes for an improved ginsenoside production. Plant Physiol Biochem 41(11):1019–1025. doi: 10.1016/j.plaphy.2003.09.002 CrossRefGoogle Scholar
  44. Patra N, Srivastava AK (2014) Enhanced production of artemisinin by hairy root cultivation of Artemisia annua in a modified stirred tank reactor. Appl Biochem Biotechnol 174(6):2209–2222. doi: 10.1007/s12010-014-1176-8 CrossRefGoogle Scholar
  45. Rahpeyma SA, Moieni A, Javaran JM (2015) Paclitaxel production is enhanced in the suspension-cultured Corylus avellana cells by using combinations of sugar, precursor, and elicitor. Eng Life Sci 15(2):234–242. doi: 10.1002/elsc.201400115 CrossRefGoogle Scholar
  46. Ramesha BT, Amna T, Ravikanth G et al (2008) Prospecting for the camptothecines from Nothapodytes nimmoniana in Western Ghats, South India: identification of high-yielding sources of camptothecin and new families of camptothecines. J Chromatogr Sci 46(4):362–368. doi: 10.1093/chromsci/46.4.362 CrossRefGoogle Scholar
  47. Ravikumar K, Ved DK (2000) 100 red-listed medicinal plants of conservation concern in South India, 1st edn. FRLHT, BangaloreGoogle Scholar
  48. Saco D, Martin S, San Jose P (2013) Vanadium distribution in roots and leaves of Phaseolus vulgaris: morphological and ultrastructural effects. Biol Plant 57(1):128–132. doi: 10.1007/s10535-012-0133-z CrossRefGoogle Scholar
  49. Saito K, Sudo H, Yamazaki M et al (2001) Feasible production of camptothecin by hairy root culture of Ophiorrhriza pumila. Plant Cell Rep 20:267–271. doi: 10.1007/s002990100320 CrossRefGoogle Scholar
  50. Sanchez-Sampedro MA, Fernandez-Tarrago J, Corchete P (2005) Yeast extract and methyl jasmonate-induced silymarin production in cell cultures of Silybum marianum (L.) Gaernt. J Biotechnol 119:60–69. doi: 10.1016/j.jbiotec.2005.06.012 CrossRefGoogle Scholar
  51. Smith JI, Smart NJ, Misawa M et al (1987) Increased accumulation of indole alkaloids by some cell lines of Catharanthus roseus in response to the addition of vanadyl sulfate. Plant Cell Rep 6(2):142–145. doi: 10.1007/BF00276673 Google Scholar
  52. Sriram D, Yogeeswar P, Thirumurugan R, Bal TR (2005) Camptothecin and its analogs: a review on their chemotherapeutic potential. Nat Products Res 19(4):393–412. doi: 10.1080/14786410412331299005 CrossRefGoogle Scholar
  53. Srivastava V, Negi AS, Kumar JK et al (2005) Plant-based anticancer molecules: a chemical and biological profile of some important leads. Bioorganic Med Chem 13:5892–5908. doi: 10.1016/j.bmc.2005.05.066 CrossRefGoogle Scholar
  54. Tallevi S, DiCosmo F (1988) Stimulation of indole alkaloid content in vanadium treated Catharanthus roseus suspension cultures. Planta Med 54:149–152. doi: 10.1055/s-2006-962374 CrossRefGoogle Scholar
  55. Uday Bhanu M, Kondap AK (2010) Neurotoxic activity of a topoisomerase-I inhibitor, camptothecin in cultured cerebellar granule neurons. Neurotoxicol 31:730–737. doi: 10.1016/j.neuro.2010.06.008 CrossRefGoogle Scholar
  56. Vanisree M, Tsay HS (2004) Plant cell cultures—an alternative and efficient source for the production of biologically important secondary metabolites. Int J Appl Sci Eng 2:29–43Google Scholar
  57. Verpoorte R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1:13–25. doi: 10.1023/A:1015871916833 CrossRefGoogle Scholar
  58. Wall ME, Wani MC, Cook CE et al (1966) Plant antitumor agents I: the isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminata. J Am Chem Soc 88:3888–3890. doi: 10.1021/ja00968a057 CrossRefGoogle Scholar
  59. Yamazaki Y, Sudo H, Yamazaki M et al (2003) Camptothecin biosynthetic genes in the hairy roots of Ophiorrhiza pumila: cloning, characterization, and differential expression in tissues and by stress compounds. Plant Cell Physiol 44(4):395–403. doi: 10.1093/pcp/pcg051 CrossRefGoogle Scholar
  60. Yan Q, Hu ZD, Wu JY (2006) Synergistic effects of biotic and abiotic elicitors on the production of tanshinones in Salvia miltiorrhiza hairy root culture. China J Chin Materia Med 31(3):188–191. doi: 10.1007/s00253-007-1332-y Google Scholar
  61. Zhao JL, Zhou LG, Wu JY (2010) Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl Microbiol Biotechnol 87(1):137–144. doi: 10.1007/s00253-010-2443-4 CrossRefGoogle Scholar
  62. Zheng Z, Wu M (2004) Cadmium treatment enhances the production of alkaloid secondary metabolites of Catharanthus roseus. Plant Sci 166:507–514. doi: 10.1016/j.plantsci.2003.10.022 CrossRefGoogle Scholar

Copyright information

© Institute of Chemistry, Slovak Academy of Sciences 2016

Authors and Affiliations

  1. 1.Cellular Differentiation and Molecular Genetics Section, Department of BotanyHamdard UniversityNew DelhiIndia

Personalised recommendations