Preparation of Dextran Aldehyde and BSA Conjugates from Ligno-cellulosic Biowaste for Antioxidant and Anti-cancer Efficacy

Abstract

The present study attempted to demonstrate the potential application of Kraft lignin (KL) from sugarcane baggasse biomass in the bio-therapeutic areas. Novel conjugate materials (Dex-ald–KL and BSA–KL) were synthesized incorporating KL into dextran aldehyde (Dex-ald) and bovine serum albumin (BSA) via a free radical reaction involving reactive oxygen species induced by ascorbic acid/H2O2 redox pair and studied using various physico-chemical techniques. UV–Visible spectral analysis of the resulting conjugates proved the enhanced conjugation (matrix formation) between constituent biopolymers due to formation of intermolecular linkages. Visual changes were observed in the X-ray diffractogram (XRD) peaks of the conjugates in comparison to free components. Cell viability of the novel conjugate materials was found to decrease by ~ 55–61% against colon cancerous cells (SW480) proving its efficacy as anti-cancer agent while the quantity of reactive oxygen species (ROS) level markedly increased on treatment with conjugate material in comparison to Dex-ald, KL and BSA alone. The above evidences indicated that the conjugates with even low amounts of lignin incorporation exhibited remarkable cytotoxicity suggesting their practical use in the treatment of certain type of cancers.

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References

  1. 1.

    Alzagameem, A., El Khaldi-Hansen, B., Büchner, D., Larkins, M., Kamm, B., Witzleben, S., Schulze, M.: Lignocellulosic biomass as source for lignin-based environmentally benign antioxidants. Molecules 23, 2664 (2018)

    Google Scholar 

  2. 2.

    Andrijevic, L.J., Radotic, K., Bogdanovic, J., Mutavdzic, D., Bogdanovic, G.: Antiproliferative effect of synthetic lignin against human breast cancer and normal fetal lung cell lines. Potency of low molecular weight fractions. J. Buon. 13, 241–244 (2008)

    Google Scholar 

  3. 3.

    Barapatre, A., Meena, A.S., Mekalac, S., Das, A., Jha, H.: In vitro evaluation of antioxidant and cytotoxic activities of lignin fractions extracted from Acacia nilotica. Int. J. Biol. Macromol. 86, 443–453 (2016)

    Google Scholar 

  4. 4.

    Barbosa, L.R.S., Ortore, M.G., Spinozzi, F., Mariani, P., Bernstorff, S., Itr, R.: The importance of protein-protein I interactions on the pH-induced conformational changes of bovine serum albumin: a small-angle X-ray scattering study. Biophys. J. 98, 147–157 (2010)

    Google Scholar 

  5. 5.

    Basu, A., Kunduru, K.R., Abtew, E., Domb, A.J.: Polysaccharide-based conjugates for biomedical applications. Bioconjugate Chem. 26, 1396–1412 (2015)

    Google Scholar 

  6. 6.

    Bhatia, L., Johri, S., Ahmad, R.: An economic and ecological perspective of ethanol production from renewable agro waste: a review. AMB Exp. 2, 1–19 (2012)

    Google Scholar 

  7. 7.

    Bhavani, A.L., Nisha, J.: Dextran—the polysaccharide with versatile uses. Int. J. Pharm. Biol. Sci. 1, 569–573 (2010)

    Google Scholar 

  8. 8.

    Campbell, M.M., Sederoff, R.R.: Variation in lignin content and composition. Plant Physiol. 11(3–1), 3 (1996)

    Google Scholar 

  9. 9.

    Cirillo, G., Kraemer, K., Fuessel, S., Puoci, F., Curcio, M., Spizzirri, U.G., Altimari, I., Iemma, F.: Biological activity of a gallic acid-gelatin conjugate. Biomacromol 11, 3309–3315 (2010)

    Google Scholar 

  10. 10.

    Dev, A., Srivastava, A.K., Roy Choudhur, S., Karmakar, S.: Nano-curcumin influences blue light photodynamic therapy for restraining glioblastoma stem cells growth. RSC Adv. 6, 95165–95168 (2016)

    Google Scholar 

  11. 11.

    Dhakal, H.N., Zhang, Z.Y., Bennett, N.: Influence of fibre treatment and glass fibre hybridisation on thermal degradation and surface energy characteristics of hemp/unsaturated polyester composites. Composites B 43, 2757–2761 (2012)

    Google Scholar 

  12. 12.

    Fernandes, E.M., Pires, R.A., Mano, J.F., Reis, R.L.: Biocomposites from lignocellulosic resources: properties, applications, and future trends for their use in biomedical field. Prog. Polym. Sci. 38, 1415–1441 (2013)

    Google Scholar 

  13. 13.

    French Alfred, D., Santiago Cintrón, M.: Cellulose polymorphy, crystallite size, and the Segal Crystallinity Index. Cellulose 20, 583–588 (2013)

    Google Scholar 

  14. 14.

    Gao, R., Lu, F., Zhu, Y., Hahn, M.G., Ralph, J.: Flexible method for conjugation of phenolic lignin model compounds to carrier proteins. J. Agric. Food Chem. 64, 7782–7788 (2016)

    Google Scholar 

  15. 15.

    Goudarzi, A., Lin, L.-T., Ko, F.K.: X-ray diffraction analysis of kraft lignins and lignin-derived carbon nanofibers. J. Nanotechnol. Eng. Med. 5, 0210061–02100615 (2014)

    Google Scholar 

  16. 16.

    Garg, P., Kumar, S., Pandey, S., Seonwoo, H., Choung, P.H., Koh, C.H.: Triphenylamine coupled chitosan with high buffering capacity and low viscosity for enhanced transfection in mammalian cells, in vitro and in vivo. J. Mater. Chem. B 1, 6053–6065 (2013)

    Google Scholar 

  17. 17.

    Glasser, W.G.: About making lignin great again—some lessons from the past. Front. Chem. 7, 565–582 (2019)

    Google Scholar 

  18. 18.

    Hatakeyama, H., Hatakeyama, T.: Lignin structure, properties, and applications. Adv. Polym. Sci. 232, 1–63 (2010)

    MATH  Google Scholar 

  19. 19.

    Hu, Q., Wang, T., Zhou, M., Xue, J., Lu, Y.: In vitro antioxidant-activity evaluation of gallic-acid-grafted chitosan conjugate synthesized by free-radical-induced grafting method. J. Agric. Food Chem. 64, 5893–5900 (2016)

    Google Scholar 

  20. 20.

    Jaiswal, S., Dutta, P.K., Kumar, S., Koh, J., Pandey, S.: Methyl methacrylate modified chitosan: synthesis, characterization and application in drug and gene delivery. Carbohydr. Polym. 211, 109–117 (2019)

    Google Scholar 

  21. 21.

    Jeyaraj, M., Praphakar, R.A., Rajendran, C., Ponnamma, D., Sadasivuni, K.K., Munusamy, M.A., Rajan, M.: Surface functionalization of natural lignin isolated from Aloe barbadensis Miller biomass by atom transfer radical polymerization for enhanced anticancer efficacy. RSC Adv. 6, 51310–51319 (2016)

    Google Scholar 

  22. 22.

    Jung, S.H., Choi, S.J., Kim, J.H., Moon, T.W.: Molecular characteristics of bovine serum albumin-dextran conjugates. Biosci. Biotechnol. Biochem. 70, 2064–2070 (2006)

    Google Scholar 

  23. 23.

    Kadla, J.F., Kubo, S., Venditti, R.A., Gilbert, R.D., Compere, A.L., Griffith, W.: Lignin-based carbon fibers for composite fiber applications. Carbon 40, 2913–2920 (2002)

    Google Scholar 

  24. 24.

    Kumar, S., Krishnakumar, B., Sobra, A.J.F.N., Koh, J.: Bio-based (chitosan/PVA/ZnO) nanocomposites film: thermally stable and photoluminescence material for removal of organic dye. Carbohydr. Polym. 205, 559–564 (2019)

    Google Scholar 

  25. 25.

    Kumar, S., Garg, P., Pandey, S., Kumari, M., Hoon, S., Je-Jang, K., Kapavarapu, R., Choung, P.H., Sobral, A.J.F.N., Chung, J.H.: Enhanced chitosan–DNA interaction by 2-acrylamido-2-methylpropane coupling for an efficient transfection in cancer cells. J. Mater. Chem. B 3, 3465–3475 (2015)

    Google Scholar 

  26. 26.

    Li, C., Xing, L., Che, S.: Coordination bonding based pH-responsive albumin nanoparticles for anticancer drug delivery. Dalton Trans. 41, 3714–3719 (2012)

    Google Scholar 

  27. 27.

    Li, D., Sun, C., Li, H., Shi, H., Shai, X., Sun, Q., Han, J., Shen, Y., Yip, H.L., Huang, F., Wang, M.: Amino-functionalized conjugated polymer electron transport layers enhance the UV photostability of planar hetero junction perovskite solar cells. Chem. Sci. 8, 4587–4594 (2017)

    Google Scholar 

  28. 28.

    Liu, F., Sun, C., Yang, W., Yuan, F., Gao, Y.: Structural characterization and functional evaluation of lactoferrin-polyphenol conjugates formed by free-radical graft copolymerization. RSC Adv. 5, 15641–15651 (2015)

    Google Scholar 

  29. 29.

    Li, Y., Sarkanen, S.: Alkylated kraft lignin-based thermoplastic blends with aliphatic polyesters. Macromolecules 35, 9707–9715 (2002)

    Google Scholar 

  30. 30.

    Masuelli, M.A.: Study of bovine serum albumin solubility in aqueous solutions by intrinsic viscosity measurements. Adv. Phys. Chem. 6, 1–7 (2013)

    Google Scholar 

  31. 31.

    Mitjans, M., Vinardell, M.P.: Biological activity and health benefits of lignans and lignins. Trends Comp. Biochem. Physiol. 11, 55–62 (2005)

    Google Scholar 

  32. 32.

    Moussawi, R.N., Patra, D.: Nanoparticle self-assembled grain like curcumin conjugated ZnO: curcumin conjugation enhances removal of perylene, fluoranthene, and chrysene by ZnO. Sci. Rep. 6, 1–13 (2016)

    Google Scholar 

  33. 33.

    Murali, S., Kumar, S., Koh, J., Seena, S., Singh, P., Ramalho, A.: Bio-based chitosan/gelatin/Ag@ZnO bionanocomposites: synthesis and mechanical and antibacterial properties. Cellulose 26, 5347–5361 (2019)

    Google Scholar 

  34. 34.

    Naessens, M., Cerdobbel, A., Soetaert, W., Vandamme, E.J.: Leuconostoc dextransucrase and dextran: production, properties and applications. J. Chem. Technol. Biotechnol. 80, 845–860 (2005)

    Google Scholar 

  35. 35.

    Nkwachukwu, O.I., Chima, C.H., Ikenna, A., Alber, L.: Focus on potential environmental issues on plastic world towards a sustainable plastic recycling in developing countries. Int. J. Ind. Chem. 4, 1–13 (2013)

    Google Scholar 

  36. 36.

    Oliver, S., Thomas, D.S., Kavallaris, M., Vittorio, O., Boyer, C.: Efficient functionalisation of dextran-aldehyde with catechin: potential applications in the treatment of cancer. Polym. Chem. 7, 2542–2552 (2016)

    Google Scholar 

  37. 37.

    Park, Y., Doherty, W.O.S., Halley, P.J.: Developing lignin-based resin coatings and composites. Ind. Crop Prod. 27, 163–167 (2008)

    Google Scholar 

  38. 38.

    Ponomarenko, J., Dizhbite, T., Lauberts, M., Volperts, A., Dobele, G., Latvian, G.T.: Analytical pyrolysis—a tool for revealing of lignin structure-antioxidant activity relationship. J. Anal. Appl. Pyrolysis 113, 360–369 (2015)

    Google Scholar 

  39. 39.

    Quinlan, G.J., Martin, G.S., Evans, T.W.: Albumin: biochemical properties and therapeutic potential. Hepatology 41, 631–637 (2005)

    Google Scholar 

  40. 40.

    Rai, S., Dutta, P.K., Mehrotra, G.K.: Agrowaste derived phenolic compounds as additives to chitosan film for food packaging applications: antibacterial and antioxidant study. J. Indian Chem. Soc. 93, 767–774 (2016)

    Google Scholar 

  41. 41.

    Rai, S., Kureel, A.K., Dutta, P.K., Mehrotra, G.K.: Phenolic compounds based conjugates from dextran aldehyde and BSA: preparation, characterization and evaluation of their anti-cancer efficacy for therapeutic applications. Int. J. Biol. Macromol. 110, 425–436 (2018)

    Google Scholar 

  42. 42.

    Rencoret, J., Nieto, A.G.L., Jimenez-Barbero, J., Faulds, C.B., Kim, H., Ralph, J., Martinez, A.T., del Rio, J.C.: Lignin composition and structure in young versus adult Eucalyptus globulus plants. Plant Physiol. 155, 667–682 (2011)

    Google Scholar 

  43. 43.

    Sahoo, S., Mishra, M., Mohanty, A.K.: Enhanced properties of lignin-based biodegradable polymer composites using injection moulding process. Composites A 42, 1710–1718 (2011)

    Google Scholar 

  44. 44.

    Satyanarayana, K.G., Arizaga, G.G.C., Wypych, F.: Biodegradable composites based on lignocellulosic fibers—an overview. Prog. Polym. Sci. 34, 982–1021 (2009)

    Google Scholar 

  45. 45.

    Singh, J., Dutta, P.K., Dutta, J., Hunt, A.J., Macquarrie, D.J., Clark, J.H.: Preparation and properties of highly soluble chitosan-l-glutamic acid aerogel derivative. Carbohydr. Polym. 76(2), 188–195 (2009)

    Google Scholar 

  46. 46.

    Singleton, V.L., Orthofer, R., Lamuela-Raventos, R.M.: Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299, 152–178 (1999)

    Google Scholar 

  47. 47.

    Soeiro, V.C., Melo, K.R.T., Alves, M.G.C.F., Medeiros, M.J.C., Grilo, M.L.P.M., Almeida-Lima, J., Pontes, D.L., Costa, L.S., Rocha, H.A.: Dextran: influence of molecular weight in antioxidant properties and immunomodulatory potential. Int. J. Mol. Sci. 17, 1340–1350 (2016)

    Google Scholar 

  48. 48.

    Srivastava, M., Singh, J., Yashpal, M., Gupta, D.K., Mishra, R.K., Tripathi, S., Ojha, A.K.: Synthesis of superparamagnetic bare Fe3O4 nanostructures and core/shell (Fe3O4/alginate) nanocomposites. Carbohydr. Polym. 89, 821–829 (2012)

    Google Scholar 

  49. 49.

    Su, H., Zhang, W., Wu, Y., Han, X., Liu, G., Jia, Q., Shan, S.: Schiff base-containing dextran nanogel as pH-sensitive drug delivery system of doxorubicin: synthesis and characterization. J. Biomater. Appl. 33(2), 170–181 (2018)

    Google Scholar 

  50. 50.

    Svensson, S.: Minimizing the Sulphur Content in Kraft Lignin. Degree Project, ECTS 30.0. STFI-Packforsk, Stockholm (2008)

    Google Scholar 

  51. 51.

    Tavernier, M.L., Petit, E., Delattre, C., Courtois, B., Courtois, J., Strancar, A., Michaud, P.: Production of oligoglucuronans using a monolithic enzymatic microreactor. Carbohydr. Res. 343, 2687–2691 (2008)

    Google Scholar 

  52. 52.

    Ugartondo, V., Mitjans, M., Vinardell, M.P.: Comparative antioxidant and cytotoxic effects of lignins from different sources. Bioresour. Technol. 99, 6683–6687 (2008)

    Google Scholar 

  53. 53.

    Upadhyaya, L., Singh, J., Agarwal, V., Pandey, A.C., Verma, S.P., Das, P., Tewari, R.P.: In situ grafted nanostructured ZnO/carboxymethyl cellulose nanocomposites for efficient delivery of curcumin to cancer. J. Polym. Res. 550, 1–9 (2014)

    Google Scholar 

  54. 54.

    Upadhyaya, L., Singh, J., Agarwal, V., Pandey, A.C., Verma, S.P., Das, P., Tewari, R.P.: Efficient water soluble nanostructured ZnO grafted O-carboxymethyl chitosan/curcumin-nanocomposite for cancer therapy. Process. Biochem. 50, 678–688 (2015)

    Google Scholar 

  55. 55.

    Vittorio, O., Cirillo, G., Iemma, F., Turi, G.D., Jacchetti, E., Curcio, M., Barbuti, S., Funel, N., Parisi, O.I., Puoci, F., Picci, N.: Dextran-catechin conjugate: a potential treatment against the pancreatic ductal adenocarcinoma. Pharm. Res. 29, 2601–2614 (2012)

    Google Scholar 

  56. 56.

    Wyman, C.E.: Biomass ethanol: technical progress, opportunities, and commercial challenges. Annu. Rev. Energy Environ. 24, 189–226 (1999)

    Google Scholar 

  57. 57.

    Zhao, C., Huang, J., Yang, L., Yue, F., Lu, F.: Revealing structural differences between alkaline and Kraft lignins by HSQC NMR. Ind. Eng. Chem. Res. 58, 5707–5714 (2019)

    Google Scholar 

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Acknowledgements

Authors thank Prof. Rajeev Tripathi, Director, Motilal Nehru National Institute of Technology Allahabad, Prayagraj, India for providing institutional facilities including instrumentation at the Center for Interdisciplinary Research. Authors are also grateful to Council of Scientific and Industrial Research (CSIR, New Delhi), Government of India, for necessary financial support to SR. Authors also gratefully acknowledged to Dr. Ruchi Chawla, Women Scientist-DST, MNNIT Allahabad for her assistance and suggestion while editing the entire manuscript.

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Rai, S., Arun, S., Kureel, A.K. et al. Preparation of Dextran Aldehyde and BSA Conjugates from Ligno-cellulosic Biowaste for Antioxidant and Anti-cancer Efficacy. Waste Biomass Valor 12, 1327–1339 (2021). https://doi.org/10.1007/s12649-020-01088-0

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Keywords

  • Lignin
  • Dextran aldehyde
  • BSA
  • ROS
  • Anti-cancer