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Characterization of Chitin-Glucan Complex of Ganoderma lucidum Extract and Its Application as Hemostatic Hydrogel

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Abstract

Chitin and glucan in the cell wall of Ganoderma lucidum have various biological activities, but are usually not effectively utilized or discarded as insoluble waste. The aim of this study is to characterize the chitin-glucan complex extracted from Ganoderma lucidum residues and to access its application potential as a hemostatic material. Ganoderma lucidum chitin-glucan complex (GLCGC) was extracted from Ganoderma lucidum, and GLCGC was prepared into a novel Ganoderma lucidum chitin-glucan complex hydrogel (GLCGCH) with ionic liquid [AMIM]Cl. GLCGC and lyophilized GLCGCH was characterized by fourier transform infrared spectroscopy, scanning electron microscope, swelling capacity, rheological properties and hemostatic properties. Our results showed that the extracted GLCGC mainly consisted of glucan (76.7 ± 2.9%) and chitin (3.85 ± 0.55%). The hydrogel GLCGCH had three-dimensional porous structure with good performance in swelling behavior (with swelling ratios of 1181.0–1891.0%). With no cytotoxicity against mouse fibroblast cells, GLCGCH showed good blood compatibility (with hemolysis ratios of 0.9–1.5%) and in vitro blood coagulation property (with blood clotting indices of 35.3–41.9%), indicating GLCGCH has great hemostatic effect. This work provided new insight into the integrated utilization of Ganoderma lucidum residues. The prepared hydrogel could be used as a promising material for hemostatic application.

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References

  1. Li, Z., Zhou, J., Lin, Z.: Development and innovation of ganoderma industry and products in China. Adv. Exp. Med. Biol. 1181, 187–204 (2019). https://doi.org/10.1007/978-981-13-9867-4_7

    Article  Google Scholar 

  2. Jiang, D., et al.: Restoration of the tumor-suppressor function to mutant p53 by ganoderma lucidum polysaccharides in colorectal cancer cells. Oncol. Rep. 37(1), 594–600 (2017). https://doi.org/10.3892/or.2016.5246

    Article  Google Scholar 

  3. Zhang, J., et al.: Toxicology and immunology of ganoderma lucidum polysaccharides in Kunming mice and wistar rats. Int. J. Biol. Macromol. 85, 302–310 (2016). https://doi.org/10.1016/j.ijbiomac.2015.12.090

    Article  Google Scholar 

  4. Gill, B.S., Gill, N., Kumar, S.: Ganoderma lucidum targeting lung cancer signaling: a review. Tumor Biol. 39(6), 1–10 (2017). https://doi.org/10.1177/1010428317707437

    Article  Google Scholar 

  5. Kurita, K.: Chitin and chitosan: functional biopolymers from marine crustaceans. Mar. Biotechnol. 8(3), 203–226 (2006). https://doi.org/10.1007/s10126-005-0097-5

    Article  Google Scholar 

  6. Jones, M.P., et al., Crab vs. mushroom: A review of crustacean and fungal chitin in wound treatment. Marine Drugs, 2020. 18(1): p. 64–88. http://dx.doi.org/https://doi.org/10.3390/md18010064.

  7. Nawawi, W.M.F.B.W., et al.: Nanomaterials derived from fungal sources—is it the new hype? Biomacromolecules 21(1), 30–55 (2020). https://doi.org/10.1021/acs.biomac.9b01141

    Article  Google Scholar 

  8. Nawawi, W.M., et al.: Plastic to elastic: fungi-derived composite nanopapers with tunable tensile properties. Compos. Sci. Technol. 198, 108327 (2020). https://doi.org/10.1016/j.compscitech.2020.108327

    Article  Google Scholar 

  9. Abdel-Mohsen, A.M., et al.: Novel chitin/chitosan-glucan wound dressing: isolation, characterization, antibacterial activity and wound healing properties. Int. J. Pharm. 510(1), 86–99 (2016). https://doi.org/10.1016/j.ijpharm.2016.06.003

    Article  Google Scholar 

  10. Janesch, J., et al.: Mushroom-derived chitosan-glucan nanopaper filters for the treatment of water. React. Funct. Polym. 146, 1–10 (2020). https://doi.org/10.1016/j.reactfunctpolym.2019.104428

    Article  Google Scholar 

  11. Yousefi, N., et al.: Fungal chitin-glucan nanopapers with heavy metal adsorption properties for ultrafiltration of organic solvents and water. Carbohyd. Polym. 253, 117273 (2021). https://doi.org/10.1016/j.carbpol.2020.117273

    Article  Google Scholar 

  12. Narayanan, K.B., Zo, S.M., Han, S.S.: Novel biomimetic chitin-glucan polysaccharide nano/microfibrous fungal-scaffolds for tissue engineering applications. Int. J. Biol. Macromol. 149, 724–731 (2020). https://doi.org/10.1016/j.ijbiomac.2020.01.276

    Article  Google Scholar 

  13. Basha, R.Y., Sampath Kumar, T.S., Doble, M.: Electrospun nanofibers of Curdlan (β-1,3 Glucan) blend as a potential skin scaffold material. Macromol. Mater. Eng. 302(4), 1600417 (2017). https://doi.org/10.1002/mame.201600417

    Article  Google Scholar 

  14. Park, J.-S., et al.: Preparation and evaluation of β-glucan hydrogel prepared by the radiation technique for drug carrier applications. Int. J. Biol. Macromol. 118(15), 333–339 (2018). https://doi.org/10.1016/j.ijbiomac.2018.06.068

    Article  Google Scholar 

  15. Shalumon, K.T., et al.: Electrospinning of carboxymethyl chitin/poly(vinyl alcohol) nanofibrous scaffolds for tissue engineering applications. Carbohyd. Polym. 77(4), 863–869 (2009). https://doi.org/10.1016/j.carbpol.2009.03.009

    Article  Google Scholar 

  16. Muzzarelli, R.A.A.: Chitins and chitosans for the repair of wounded skin, nerve, cartilage and bone. Carbohyd. Polym. 76(2), 167–182 (2009). https://doi.org/10.1016/j.carbpol.2008.11.002

    Article  Google Scholar 

  17. Klokkevold, P.R., et al.: The effect of chitosan (poly-N-acetyl glucosamine) on lingual hemostasis in heparinized rabbits. J. Oral Maxillofac. Surg. 57(1), 49–52 (1999). https://doi.org/10.1016/S0278-2391(99)90632-8

    Article  Google Scholar 

  18. Zhang, W., Sun, Y.-L., Chen, D.-H.: Effects of chitin and sepia ink hybrid hemostatic sponge on the blood parameters of mice. Mar. Drugs 12(4), 2269–2281 (2014). https://doi.org/10.3390/md12042269

    Article  Google Scholar 

  19. Usami, Y., et al.: Influence of chain length of N-acetyl-D-glucosamine and D-glucosamine residues on direct and complement-mediated chemotactic activities for canine polymorphonuclear cells. Carbohyd. Polym. 32(2), 115–122 (1997). https://doi.org/10.1016/S0144-8617(96)00153-1

    Article  MathSciNet  Google Scholar 

  20. Ueno, H., et al.: Accelerating effects of chitosan for healing at early phase of experimental open wound in dogs. Biomaterials 20(15), 1407–1414 (1999). https://doi.org/10.1016/S0142-9612(99)00046-0

    Article  Google Scholar 

  21. Zhou, H.Y., et al.: Glycerophosphate-based chitosan thermosensitive hydrogels and their biomedical applications. Carbohyd. Polym. 117(6), 524–536 (2015). https://doi.org/10.1016/j.carbpol.2014.09.094

    Article  Google Scholar 

  22. Lan, G., et al.: Chitosan/gelatin composite sponge is an absorbable surgical hemostatic agent. Colloids Surf. B 136, 1026–1034 (2015). https://doi.org/10.1016/j.colsurfb.2015.10.039

    Article  Google Scholar 

  23. Liu, J.-Y., et al.: Hemostatic porous sponges of cross-linked hyaluronic acid/cationized dextran by one self-foaming process. Mater. Sci. Eng. C 83, 160–168 (2018). https://doi.org/10.1016/j.msec.2017.10.007

    Article  Google Scholar 

  24. Ferreira, I.C., et al.: Chitin-glucan complex - based biopolymeric structures using biocompatible ionic liquids. Carbohyd. Polym. 247, 116679 (2020). https://doi.org/10.1016/j.carbpol.2020.116679

    Article  Google Scholar 

  25. Farinha, I., et al.: Chitin–glucan complex production by Komagataella pastoris: downstream optimization and product characterization. Carbohyd. Polym. 130, 455–464 (2015). https://doi.org/10.1016/j.carbpol.2015.05.034

    Article  Google Scholar 

  26. Hu, X., et al.: Solubility and property of chitin in NaOH/urea aqueous solution. Carbohyd. Polym. 70(4), 451–458 (2007). https://doi.org/10.1016/j.carbpol.2007.05.002

    Article  Google Scholar 

  27. Zhang, J., et al.: Application of ionic liquids for dissolving cellulose and fabricating cellulose-based materials: state of the art and future trends. Mater. Chem. Front. 1, 1273–1290 (2017). https://doi.org/10.1039/C6QM00348F

    Article  Google Scholar 

  28. Poirier, M., Charlet, G.: Chitin fractionation and characterization in N, N-dimethylacetamide/lithium chloride solvent system. Carbohyd. Polym. 50(4), 363–370 (2002). https://doi.org/10.1016/S0144-8617(02)00040-1

    Article  Google Scholar 

  29. Yao, Z.C., et al.: Ganoderma lucidum polysaccharide loaded sodium alginate micro-particles prepared via electrospraying in controlled deposition environments. Int. J. Pharm. 524(1), 148–158 (2017). https://doi.org/10.1016/j.ijpharm.2017.03.064

    Article  Google Scholar 

  30. Mokhtari-Hosseini, Z.B., et al.: Chitin and chitosan biopolymer production from the Iranian medicinal fungus ganoderma lucidum: optimization and characterization. Prep. Biochem. Biotechnol. 48(7), 662–670 (2018). https://doi.org/10.1080/10826068.2018.1487847

    Article  Google Scholar 

  31. Wu, T., et al.: Chitin and chitosan value-added products from mushroom waste. J. Agric. Food Chem. 52(26), 7905–7910 (2004). https://doi.org/10.1021/jf0492565

    Article  Google Scholar 

  32. Elson, L.A., Morgan, W.T.: A colorimetric method for the determination of glucosamine and chondrosamine. Biochem. J. 27(6), 1824–1828 (1933). https://doi.org/10.1042/bj0271824

    Article  Google Scholar 

  33. Dimzon, I.K.D., Knepper, T.P.: Degree of deacetylation of chitosan by infrared spectroscopy and partial least squares. Int. J. Biol. Macromol. 72, 939–945 (2015). https://doi.org/10.1016/j.ijbiomac.2014.09.050

    Article  Google Scholar 

  34. Sluiter, A., et al.: Determination of structural carbohydrates and lignin in biomass, Technical Report NREL/TP-510–42618, National Renewable Energy Laboratory, Golden, CO. 2010.

  35. Zhang, F., et al.: Fibrous aramid hydrogel supported antibacterial agents for accelerating bacterial-infected wound healing. Mater. Sci. Eng., C 121, 111833 (2021). https://doi.org/10.1016/j.msec.2020.111833

    Article  Google Scholar 

  36. Wang, S., et al.: Study of double-bonded carboxymethyl chitosan/cysteamine-modified chondroitin sulfate composite dressing for hemostatic application. Eur. Polymer J. 162, 110875 (2022). https://doi.org/10.1016/j.eurpolymj.2021.110875

    Article  Google Scholar 

  37. Liu, X., et al.: Rapid hemostatic and mild polyurethane-urea foam wound dressing for promoting wound healing. Mater. Sci. Eng. C 71, 289–297 (2017). https://doi.org/10.1016/j.msec.2016.10.019

    Article  Google Scholar 

  38. Su, C.H., et al.: Fungal mycelia as the source of chitin and polysaccharides and their applications as skin substitutes. Biomaterials 18(17), 1169–1174 (1997). https://doi.org/10.1016/S0142-9612(97)00048-3

    Article  Google Scholar 

  39. Vetter, J.: Chitin content of cultivated mushrooms agaricus bisporus, pleurotus ostreatus and lentinula edodes. Food Chem. 102(1), 6–9 (2007). https://doi.org/10.1016/j.foodchem.2006.01.037

    Article  Google Scholar 

  40. Zhang, P., Sutheerawattananonda, M.: Kinetic models for glucosamine production by acid hydrolysis of chitin in five mushrooms. Int. J. Chem. Eng. 2020, 1–8 (2020). https://doi.org/10.1155/2020/5084036

    Article  Google Scholar 

  41. Sun, C., et al.: Chitin isolated from yeast cell wall induces the resistance of tomato fruit to Botrytis cinerea. Carbohyd. Polym. 199, 341–352 (2018). https://doi.org/10.1016/j.carbpol.2018.07.045

    Article  Google Scholar 

  42. Paulino, A.T., et al.: Characterization of chitosan and chitin produced from silkworm crysalides. Carbohyd. Polym. 64(1), 98–103 (2006). https://doi.org/10.1016/j.carbpol.2005.10.032

    Article  Google Scholar 

  43. Hong, Y., Ying, T.: Characterization of a chitin-glucan complex from the fruiting body of Termitomyces albuminosus (Berk.) Heim. Int. J. Biol. Macromol. (2019). https://doi.org/10.1016/j.ijbiomac.2019.04.198

    Article  Google Scholar 

  44. Boureghda, Y., Satha, H., Bendebane, F.: Chitin-glucan complex from Pleurotus ostreatus mushroom: physicochemical characterization and comparison of extraction methods. Waste Biomass Valoriz. (2021). https://doi.org/10.1007/s12649-021-01449-3

    Article  Google Scholar 

  45. Zhang, H., et al.: 1-allyl-3-methylimidazolium chloride room temperature ionic liquid: a new and powerful nonderivatizing solvent for cellulose. Macromolecules 38(20), 8272–8277 (2005). https://doi.org/10.1021/ma0505676

    Article  Google Scholar 

  46. Zainal, S.H., et al.: Preparation of cellulose-based hydrogel: a review. J. Market. Res. 10, 935–952 (2021). https://doi.org/10.1016/j.jmrt.2020.12.012

    Article  Google Scholar 

  47. Liao, J., Huang, H.: A fungal chitin derived from hericium erinaceus residue: dissolution, gelation and characterization. Int. J. Biol. Macromol. 152(1), 456–464 (2020). https://doi.org/10.1016/j.carbpol.2019.05.074

    Article  Google Scholar 

  48. Liao, J., Huang, H.: Magnetic chitin hydrogels prepared from hericium erinaceus residues with tunable characteristics: a novel biosorbent for Cu2+ removal. Carbohyd. Polym. 220(15), 191–201 (2019). https://doi.org/10.1016/j.carbpol.2019.05.074

    Article  Google Scholar 

  49. Reh, A., et al.: Efficient wound healing composite hydrogel using Egyptian Avena sativa L. polysaccharide containing β-glucan. Int. J. Biol. Macromol. 149, 1331–1338 (2020). https://doi.org/10.1016/j.ijbiomac.2019.11.046

    Article  Google Scholar 

  50. Abdel-Mohsen, A., et al.: Chitosan-glucan complex hollow fibers reinforced collagen wound dressing embedded with Aloe vera. Part I: preparation and characterization. Carbohyd. Polym. 230, 115708 (2020). https://doi.org/10.1016/j.carbpol.2019.115708

    Article  Google Scholar 

  51. Abdel-Mohsen, A., et al.: Chitosan-glucan complex hollow fibers reinforced collagen wound dressing embedded with Aloe vera. II. Multifunctional properties to promote cutaneous wound healing. Int. J. Pharm. 582, 119349 (2020). https://doi.org/10.1016/j.ijpharm.2020.119349

    Article  Google Scholar 

  52. Ahmad, S.I., et al.: Chitin and its derivatives: structural properties and biomedical applications. Int. J. Biol. Macromol. 164(1), 526–539 (2020). https://doi.org/10.1016/j.ijbiomac.2020.07.098

    Article  Google Scholar 

  53. Khan, A.A., et al.: Biological and pharmaceutical activities of mushroom β-glucan discussed as a potential functional food ingredient. Bioactive Carbohydr. Dietary Fibre 16, 1–13 (2018). https://doi.org/10.1016/j.bcdf.2017.12.002

    Article  Google Scholar 

  54. Han, F., et al.: Preparation, characteristics and assessment of a novel gelatin–chitosan sponge scaffold as skin tissue engineering material. Int. J. Pharm. 476(1), 124–133 (2014). https://doi.org/10.1016/j.ijpharm.2014.09.036

    Article  Google Scholar 

  55. Yang, X., et al.: Fabricating antimicrobial peptide-immobilized starch sponges for hemorrhage control and antibacterial treatment. Carbohyd. Polym. 222, 115012 (2019). https://doi.org/10.1016/j.carbpol.2019.115012

    Article  Google Scholar 

  56. Huang, M.H., Yang, M.C.: Evaluation of glucan/poly(vinyl alcohol) blend wound dressing using rat models. Int. J. Pharm. 346(1), 38–46 (2008). https://doi.org/10.1016/j.ijpharm.2007.06.021

    Article  Google Scholar 

  57. Howling, G.I., et al.: The effect of chitin and chitosan on the proliferation of human skin fibroblasts and keratinocytes in vitro. Biomaterials 22(22), 2959–2966 (2001). https://doi.org/10.1016/S0142-9612(01)00042-4

    Article  Google Scholar 

  58. Hattori, H., Ishihara, M.: Changes in blood aggregation with differences in molecular weight and degree of deacetylation of chitosan. Biomed. Mater. 10(1), 1015014 (2015)

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key R&D Program of China (2019YFD0901805), the 111 Project (B18022), the Fundamental Research Funds for the Central Universities, and the Open Project Funding of the State Key Laboratory of Bioreactor Engineering, ECUST (ZDXM2019). We acknowledge Yuan Li for the assistance in performing the cytotoxicity experiments.

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Liming Zhao conceived and supervised the project. Yanqiong Liu and Chunyue Zhang designed the experiments. Yanqiong Liu, Chunyue Zhang, Xingxing Zhang and Yanying Hou performed the experiments. Yanqiong Liu, Chunyue Zhang, Lujie Liu wrote the manuscript.

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Correspondence to Liming Zhao.

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Supplementary file1 (DOCX 34 kb)

12649_2022_1711_MOESM2_ESM.tif

Fig. S1 Chromatograms of glucosamine (GlcN, A), Chitobiose ([GlcN]2, B), Chitotrise ([GlcN]3, C), Chitotetraose ([GlcN]4, D) in Ganoderma lucidum chitin-glucan complex (GLCGC). In this mode, the molecular mass of [GlcN]1-4 was 180.1, 341.2, 502.2 and 663.3, respectively. Supplementary file2 (TIF 15451 kb)

12649_2022_1711_MOESM3_ESM.tif

Fig. S2 ATR-FTIR spectra of Ganoderma lucidum chitin-glucan complex (GLCGC) and Ganoderma lucidum chitin-glucan complex hydrogels GLCGCH 3, 4, 5. Supplementary file3 (TIF 475 kb)

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Liu, Y., Zhang, C., Liu, L. et al. Characterization of Chitin-Glucan Complex of Ganoderma lucidum Extract and Its Application as Hemostatic Hydrogel. Waste Biomass Valor 13, 3297–3308 (2022). https://doi.org/10.1007/s12649-022-01711-2

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