Advertisement

Cellulose

, Volume 23, Issue 5, pp 3187–3198 | Cite as

In vitro biodegradability of bacterial cellulose by cellulase in simulated body fluid and compatibility in vivo

  • Baoxiu Wang
  • Xiangguo Lv
  • Shiyan Chen
  • Zhe Li
  • Xiaoxiao Sun
  • Chao Feng
  • Huaping Wang
  • Yuemin Xu
Original Paper

Abstract

Bacterial cellulose (BC) has great potential for use as a tissue scaffold due to its unique structure and properties including high tensile strength and good biocompatibility. However, poor biodegradability of BC in the human body may be a key disadvantage limiting its application in the field. In this paper, we developed a simple absorption method to prepare biodegradable cellulase/BC materials. The morphology, structure, degradation ratio and mechanical properties during the degradation process were characterized and investigated. In vitro studies reveal that the BC material degraded gradually in simulated body fluid within 24 weeks and the degradation rate could be adjusted by modulating the cellulase content. The mechanical properties indicate the cellulase/BC material could maintain tensile strength for as long as 24 days during the degradation process. Muscle-derived cells were seeded on the cellulase/BC material to evaluate the cytotoxicity, using LIVE/DEAD® viability/cytotoxicity assay and H&E staining. In vivo biocompatibility was evaluated by subcutaneous implantation using a dog model for 1, 2, 3 and 4 weeks. These results demonstrate that the cellulase/BC material had good in vitro and in vivo biocompatibility.

Keywords

Bacterial cellulose Cellulase Biodegradation Tissue scaffold 

Notes

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (51273043, 51573024 and 81370795), the Fundamental Research Funds for the Central Universities and DHU Distinguished Young Professor Program.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

10570_2016_993_MOESM1_ESM.docx (468 kb)
Supplementary material 1 (DOCX 467 kb)

References

  1. Alvarez O, Patel M, Booker J, Markowitz L (2004) Effectiveness of a biocellulose wound dressing for the treatment of chronic venous leg ulcers: results of a single center randomized study involving 24 patients. Wounds 16:224–233Google Scholar
  2. Atala A (1997) Tissue engineering in the genitourinary system. Synthetic biodegradable polymer scaffolds. Birkhäuser, Boston, pp 149–164CrossRefGoogle Scholar
  3. Bäckdahl H, Helenius G, Bodin A, Nannmark U, Johansson BR, Risberg B, Gatenholm P (2006) Mechanical properties of bacterial cellulose and interactions with smooth muscle cells. Biomaterials 27:2141–2149CrossRefGoogle Scholar
  4. Bäckdahl H, Risberg B, Gatenholm P (2011) Observations on bacterial cellulose tube formation for application as vascular graft. Mater Sci Eng, C 31:14–21CrossRefGoogle Scholar
  5. Béguin P, Aubert JP (1994) The biological degradation of cellulose. FEMS Microbiol Rev 13:25–58CrossRefGoogle Scholar
  6. Bodin A, Bharadwaj S, Wu S, Gatenholm P, Atala A, Zhang Y (2010) Tissue-engineered conduit using urine-derived stem cells seeded bacterial cellulose polymer in urinary reconstruction and diversion. Biomaterials 31:8889–8901CrossRefGoogle Scholar
  7. Brown AJ (1886) XLIII. On an acetic ferment which forms cellulose. J Chem Soc, Faraday Trans 49:432–439CrossRefGoogle Scholar
  8. Catchmark JM, Fugmann B, Hu Y (2010) Degradable biomolecule compositions. Google patents, US 2010/0172889 A1Google Scholar
  9. Czaja W, Kyryliouk D, DePaula CA, Buechter DD (2014) Oxidation of γ-irradiated microbial cellulose results in bioresorbable, highly conformable biomaterial. J Appl Polym Sci 131:39995–40006CrossRefGoogle Scholar
  10. Endo K, Hakamada Y, Takizawa S, Kubota H, Sumitomo N, Kobayashi T, Ito S (2001) A novel alkaline endoglucanase from an alkaliphilic Bacillus isolate: enzymatic properties, and nucleotide and deduced amino acid sequences. Appl Microbiol Biotechnol 57:109–116CrossRefGoogle Scholar
  11. Gusakov AV, Salanovich TN, Antonov AI, Ustinov BB, Okunev ON, Burlingame R, Emalfarb M, Baez M, Sinitsyn AP (2007) Design of highly efficient cellulase mixtures for enzymatic hydrolysis of cellulose. Biotechnol Bioeng 97:1028–1038CrossRefGoogle Scholar
  12. Helenius G, Bäckdahl H, Bodin A, Nannmark U, Gatenholm P, Risberg B (2006) In vivo biocompatibility of bacterial cellulose. J Biomed Mater Res A 76:431–438CrossRefGoogle Scholar
  13. Hu Y, Catchmark JM (2011a) In vitro biodegradability and mechanical properties of bioabsorbable bacterial cellulose incorporating cellulases. Acta Biomater 7:2835–2845CrossRefGoogle Scholar
  14. Hu Y, Catchmark JM (2011b) Integration of cellulases into bacterial cellulose: toward bioabsorbable cellulose composites. J Biomed Mater Res B 97:114–123CrossRefGoogle Scholar
  15. Hu W, Liu S, Chen S, Wang H (2011) Preparation and properties of photochromic bacterial cellulose nanofibrous membranes. Cellulose 18:655–661CrossRefGoogle Scholar
  16. Huang Y, Zhu C, Yang J, Nie Y, Chen C, Sun D (2014) Recent advances in bacterial cellulose. Cellulose 21:1–30CrossRefGoogle Scholar
  17. Jeffries T, Eveleigh D, Macmillan J, Parrish F, Reese E (1977) Enzymatic hydrolysis of the walls of yeasts cells and germinated fungal spores. BBA Gen Subj 499:10–23CrossRefGoogle Scholar
  18. Klemm D, Schumann D, Udhardt U, Marsch S (2001) Bacterial synthesized cellulose-artificial blood vessels for microsurgery. Prog Polym Sci 26:1561–1603CrossRefGoogle Scholar
  19. Kokubo T, Takadama H (2006) How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27:2907–2915CrossRefGoogle Scholar
  20. Kokubo T, Kushitani H, Sakka S, Kitsugi T, Yamamuro T (1990) Solutions able to reproduce in vivo surface-structure changes in bioactive glass-ceramic A-W3. J Biomed Mater Res 24:721–734CrossRefGoogle Scholar
  21. Li J, Wan Y, Li L, Liang H, Wang J (2009) Preparation and characterization of 2,3-dialdehyde bacterial cellulose for potential biodegradable tissue engineering scaffolds. Mater Sci Eng, C 29:1635–1642CrossRefGoogle Scholar
  22. Li Z, Wang L, Chen S, Feng C, Chen S, Yin N, Yang J, Wang H, Xu Y (2015) Facilely green synthesis of silver nanoparticles into bacterial cellulose. Cellulose 22:373–383CrossRefGoogle Scholar
  23. Liu S-L, Chen W-Z, Wang Y, Liu G, Yu S-W, Xing M (2008) Purification and characterization of a novel neutral β-glucanase and an alkaline β-glucanase from an alkaliphilic Bacillus isolate. World J Microbiol Biotechnol 24:149–155CrossRefGoogle Scholar
  24. Maurel W, Thalmann D, Wu Y, Thalmann NM (1998) Constitutive modeling. Biomechanical models for soft tissue simulation. Springer, Berlin, pp 79–120CrossRefGoogle Scholar
  25. Mergenthaler P, Lindauer U, Dienel GA, Meisel A (2013) Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci 36:587–597CrossRefGoogle Scholar
  26. Müller D, Rambo C, Recouvreux D, Porto L, Barra G (2011) Chemical in situ polymerization of polypyrrole on bacterial cellulose nanofibers. Synth Met 161:106–111CrossRefGoogle Scholar
  27. Nakanishi Y, Chen G, Komuro H, Ushida T, Kaneko S, Tateishi T, Kaneko M (2003) Tissue-engineered urinary bladder wall sing PLGA mesh-collagen hybrid scaffolds: a comparison study of collagen sponge and gel as a caffold. J Pediatr Surg 38:1781–1784CrossRefGoogle Scholar
  28. Ni J, Wang M (2002) In vitro evaluation of hydroxyapatite reinforced polyhydroxybutyrate composite. Mater Sci Eng, C 20:101–109CrossRefGoogle Scholar
  29. Park S, Baker JO, Himmel ME, Parilla PA, Johnson DK (2010) Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance. Biotechnol Biofuels 3:1CrossRefGoogle Scholar
  30. Peng S, Zheng Y, Wu J, Wu Y, Ma Y, Song W, Xi T (2012) Preparation and characterization of degradable oxidized bacterial cellulose reacted with nitrogen dioxide. Polym Bull 68:415–423CrossRefGoogle Scholar
  31. Pértile RA, Moreira S, Gil da Costa RM, Correia A, Guãrdao L, Gartner F, Vilanova M, Gama M (2012) Bacterial cellulose: long-term biocompatibility studies. J Biomater Sci Polym Ed 23:1339–1354Google Scholar
  32. Petersen N, Gatenholm P (2011) Bacterial cellulose-based materials and medical devices: current state and perspectives. Appl Microbiol Biotechnol 91:1277–1286CrossRefGoogle Scholar
  33. Schumann DA, Wippermann J, Klemm DO, Kramer F, Koth D, Kosmehl H, Wahlers T, Salehi-Gelani S (2009) Artificial vascular implants from bacterial cellulose: preliminary results of small arterial substitutes. Cellulose 16:877–885CrossRefGoogle Scholar
  34. Scrivener A, Zhao L, Slaytor M (1997) Biochemical and immunological relationships between endo-β-1, 4-glucanases from cockroaches. Comp Biochem Physiol B: Biochem Mol Biol 118:837–843CrossRefGoogle Scholar
  35. Svensson A, Nicklasson E, Harrah T, Panilaitis B, Kaplan D, Brittberg M, Gatenholm P (2005) Bacterial cellulose as a potential scaffold for tissue engineering of cartilage. Biomaterials 26:419–431CrossRefGoogle Scholar
  36. Tanaka T, Takahashi M, Nitta N, Furukawa A, Andoh A, Saito Y, Fujiyama Y, Murata K (2006) Newly developed biodegradable stents for benign gastrointestinal tract stenoses: a preliminary clinical trial. Digestion 74:199–205CrossRefGoogle Scholar
  37. Vitta S, Drillon M, Derory A (2010) Magnetically responsive bacterial cellulose: synthesis and magnetic studies. J Appl Phys 108:053905CrossRefGoogle Scholar
  38. Walker L, Wilson D (1991) Enzymatic hydrolysis of cellulose: an overview. Bioresour Technol 36:3–14CrossRefGoogle Scholar
  39. Wang J, Zhu Y, Du J (2011) Bacterial cellulose: a natural nanomaterial for biomedical applications. J Mech Med Biol 11:285–306CrossRefGoogle Scholar
  40. Watanabe K, Tabuchi M, Morinaga Y, Yoshinaga F (1998) Structural features and properties of bacterial cellulose produced in agitated culture. Cellulose 5:187–200CrossRefGoogle Scholar
  41. Yang J, Lv X, Chen S, Li Z, Feng C, Wang H, Xu Y (2014) In situ fabrication of a microporous bacterial cellulose/potato starch composite scaffold with enhanced cell compatibility. Cellulose 21:1823–1835CrossRefGoogle Scholar
  42. Yin N, Stilwell MD, Santos TM, Wang H, Weibel DB (2015) Agarose particle-templated porous bacterial cellulose and its application in cartilage growth in vitro. Acta Biomater 12:129–138CrossRefGoogle Scholar
  43. Yu L, Lin J, Tian F, Li X, Bian F, Wang J (2014) Cellulose nanofibrils generated from jute fibers with tunable polymorphs and crystallinity. J Mater Chem A 2:6402–6411CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.State Key Laboratory for Modification of Chemical Fibers and Polymer Materials, Key Laboratory of Textile Science and Technology (Ministry of Education), College of Materials Science and EngineeringDonghua UniversityShanghaiPeople’s Republic of China
  2. 2.Department of Urology, Affiliated Sixth People’s HospitalShanghai Jiaotong UniversityShanghaiPeople’s Republic of China

Personalised recommendations