Skip to main content

Advertisement

Log in

Calcium phosphate and calcium carbonate mineralization of bioinspired hydrogels based on β-chitin isolated from biomineral of the common cuttlefish (Sepia officinalis, L.)

  • ORIGINAL PAPER
  • Published:
Journal of Polymer Research Aims and scope Submit manuscript

Abstract

Chitin, a bioactive, antibacterial and biodegradable polymer is commonly utilized by diverse marine organisms as the main scaffold material during biomineralization. Due to its properties, chitin is also of interest as a component of organo-inorganic composites for diverse biomedical applications. In this study, chitinous fibers isolated from the cuttlebone of the common cuttlefish (Sepia officinalis, L.) are characterized and evaluated for use as an integral part of mineralized hydrogels for biomedical applications. Since marine organisms use calcium carbonates (CaCO3), while vertebrates use calcium phosphates (CaP) as the main inorganic hard tissue components, and both minerals are used in hard tissue engineering, they were compared to determine which composite is potentially a better biomaterial. Hydrogel mineralization was conducted by subsequent dipping into cationic and anionic reactant solutions, resulting in the formation of a CaCO3 or CaP coating that penetrated into the hydrogel. Obtained composites were characterized by X-ray diffraction (XRD), Fourier transform infrared spectroscopy (FTIR), atomic force microscopy (AFM), scanning electron microscopy (SEM), rheology, swelling tests and simple compression. The results indicate that β-chitin can be used for the preparation of moldable hydrogels that are easily mineralized. Mineralized hydrogels have higher elasticity than non-mineralized ones while swelling is better if the extent of mineralization is lower. Further optimization of the hydrogels composition could improve their stress response and Young’s modulus, where the current hydrogel with a higher extent of CaP mineralization excels in comparison to all other investigated composites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Azuma K, Izumi R, Osaki T et al (2015) Chitin, chitosan, and its derivatives for wound healing: old and new materials. J Funct Biomater 6:104–142. https://doi.org/10.3390/jfb6010104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bentov S, Aflalo ED, Tynyakov J et al (2016) Calcium phosphate mineralization is widely applied in crustacean mandibles. Sci Rep 6. https://doi.org/10.1038/srep22118

  3. Birchall JD, Thomas NL (1983) On the architecture and function of cuttlefish bone. J Mater Sci 18:2081–2086. https://doi.org/10.1007/BF00555001

    Article  CAS  Google Scholar 

  4. Brečević L, Füredi-Milhofer H (1972) Precipitation of calcium phosphates from electrolyte solutions. Calcif Tissue Res 10:82–90. https://doi.org/10.1007/BF02012538

    Article  PubMed  Google Scholar 

  5. Buljan Meić I, Kontrec J, Domazet Jurašin D et al (2017) Comparative study of calcium carbonates and calcium phosphates precipitation in model systems mimicking the inorganic environment for biomineralization. Cryst Growth Des 17:1103–1117. https://doi.org/10.1021/acs.cgd.6b01501

    Article  CAS  Google Scholar 

  6. Čadež V, Škapin SD, Leonardi A et al (2017) Formation and morphogenesis of a cuttlebone’s aragonite biomineral structures for the common cuttlefish (Sepia officinalis) on the nanoscale: revisited. J Colloid Interface Sci 508:95–104. https://doi.org/10.1016/j.jcis.2017.08.028

    Article  CAS  PubMed  Google Scholar 

  7. Casciani F, Condrate RAS (1979) The vibrational spectra of Brushite, CaHPO4·2H2O. Spectrosc Lett 12:699–713. https://doi.org/10.1080/00387017908069196

    Article  CAS  Google Scholar 

  8. Chirapart A, Ohno M, Ukeda H et al (1995) Chemical composition of agars from a newly reported Japanese agarophyte, Gracilariopsis lemaneiformis. J Appl Phycol 7:359–365. https://doi.org/10.1007/BF00003793

    Article  CAS  Google Scholar 

  9. Christiaen D, Bodard M (1983) Spectroscopie Infrarouge de Films d’agar de Gracilaria Verrucosa (Huds.) Papenfuss. Bot Mar 26:425–428. https://doi.org/10.1515/botm.1983.26.9.425

    Article  CAS  Google Scholar 

  10. Clarke SA, Walsh P, Maggs CA, Buchanan F (2011) Designs from the deep: marine organisms for bone tissue engineering. Biotechnol Adv 29:610–617. https://doi.org/10.1016/j.biotechadv.2011.04.003

    Article  CAS  PubMed  Google Scholar 

  11. Denton EJ, Gilpin-Brown JB (1961) The Buoyancy of the Cuttlefish, Sepia officinalis (L.). J Mar Biol Assoc U K 41:319. https://doi.org/10.1017/S0025315400023948

    Article  Google Scholar 

  12. Dorozhkin SV (2009) Calcium orthophosphates in nature, biology and medicine. Materials 2:399–498. https://doi.org/10.3390/ma2020399

    Article  CAS  PubMed Central  Google Scholar 

  13. Ehrlich H (2010) Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev 52:661–699. https://doi.org/10.1080/00206811003679521

    Article  Google Scholar 

  14. El-hefian EA, Nasef MM, Yahaya AH (2012) Preparation and characterization of chitosan/agar blended films: part 1. Chemical structure and morphology. J Chem 9:141–1439. https://doi.org/10.1155/2012/781206

    Article  CAS  Google Scholar 

  15. Florek M, Fornal E, Gómez-Romero P et al (2009) Complementary microstructural and chemical analyses of Sepia officinalis endoskeleton. Mater Sci Eng C 29:1220–1226. https://doi.org/10.1016/j.msec.2008.09.040

    Article  CAS  Google Scholar 

  16. Focher B, Naggi A, Torri G et al (1992) Structural differences between chitin polymorphs and their precipitates from solutions—evidence from CP-MAS 13C-NMR, FT-IR and FT-Raman spectroscopy. Carbohydr Polym 17:97–102. https://doi.org/10.1016/0144-8617(92)90101-U

    Article  CAS  Google Scholar 

  17. Füredi-Milhofer H, Oljica-Žabčić E, Purgarić B et al (1975) Precipitation of calcium phosphates from electrolyte solutions—IV: precipitation diagrams of the system calcium chloride-sodium phosphate-0·15 M sodium chloride. J Inorg Nucl Chem 37:2047–2051. https://doi.org/10.1016/0022-1902(75)80827-X

    Article  Google Scholar 

  18. Hoseini MHM, Moradi M, Alimohammadian MH et al (2016) Immunotherapeutic effects of chitin in comparison with chitosan against Leishmania major infection. Parasitol Int 65:99–104. https://doi.org/10.1016/j.parint.2015.10.007

    Article  CAS  PubMed  Google Scholar 

  19. Ianiro A, Giosia MD, Fermani S et al (2014) Customizing properties of β-chitin in squid pen (gladius) by chemical treatments. Mar Drugs 12:5979–5992. https://doi.org/10.3390/md12125979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jang M-K, Kong B-G, Jeong Y-I et al (2004) Physicochemical characterization of α-chitin, β-chitin, and γ-chitin separated from natural resources. J Polym Sci Part Polym Chem 42:3423–3432. https://doi.org/10.1002/pola.20176

    Article  CAS  Google Scholar 

  21. Jayakumar R, Prabaharan M, Nair SV et al (2010) Novel carboxymethyl derivatives of chitin and chitosan materials and their biomedical applications. Prog Mater Sci 55:675–709. https://doi.org/10.1016/j.pmatsci.2010.03.001

    Article  CAS  Google Scholar 

  22. Jeong K-H, Park D, Lee Y-C (2017) Polymer-based hydrogel scaffolds for skin tissue engineering applications: a mini-review. J Polym Res 24:112. https://doi.org/10.1007/s10965-017-1278-4

    Article  CAS  Google Scholar 

  23. Jung H-S, Kim MH, Shin JY et al (2018) Electrospinning and wound healing activity of β-chitin extracted from cuttlefish bone. Carbohydr Polym 193:205–211. https://doi.org/10.1016/j.carbpol.2018.03.100

    Article  CAS  PubMed  Google Scholar 

  24. Kawata M, Azuma K, Izawa H et al (2016) Biomineralization of calcium phosphate crystals on chitin nanofiber hydrogel for bone regeneration material. Carbohydr Polym 136:964–969. https://doi.org/10.1016/j.carbpol.2015.10.009

    Article  CAS  PubMed  Google Scholar 

  25. Kaya M, Sargin I, Aylanc V et al (2016) Comparison of bovine serum albumin adsorption capacities of α-chitin isolated from an insect and β-chitin from cuttlebone. J Ind Eng Chem 38:146–156. https://doi.org/10.1016/j.jiec.2016.04.015

    Article  CAS  Google Scholar 

  26. Kim S-K (2013) Chitin and chitosan derivatives: advances in drug discovery and developments. CRC Press

  27. Kumar PTS, Abhilash S, Manzoor K et al (2010) Preparation and characterization of novel β-chitin/nanosilver composite scaffolds for wound dressing applications. Carbohydr Polym 80:761–767. https://doi.org/10.1016/j.carbpol.2009.12.024

    Article  CAS  Google Scholar 

  28. Kumirska J, Czerwicka M, Kaczyński Z et al (2010) Application of spectroscopic methods for structural analysis of chitin and chitosan. Mar Drugs 8:1567–1636. https://doi.org/10.3390/md8051567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mack I, Hector A, Ballbach M et al (2015) The role of chitin, chitinases, and chitinase-like proteins in pediatric lung diseases. Mol Cell Pediatr 2. https://doi.org/10.1186/s40348-015-0014-6

  30. Mahanta AK, Maiti P (2016) Chitin and chitosan Nanocomposites for tissue engineering. In: Chitin and Chitosan for Regenerative Medicine. Springer India, pp 123–149. https://doi.org/10.1007/978-81-322-2511-9_6

    Google Scholar 

  31. Mann S (2001) Biomineralization: principles and concepts in bioinorganic materials chemistry. Oxford University Press, Oxford

    Google Scholar 

  32. Marin F, Le Roy N, Marie B (2012) The formation and mineralization of mollusk shell. Front Biosci Sch Ed 4:1099–1125

    Article  Google Scholar 

  33. Miyazawa T, Fukushima K, Ideguchi Y (1962) Molecular vibrations and structure of high polymers. III. Polarized infrared spectra, Normal vibrations, and helical conformation of polyethylene glycol. J Chem Phys 37:2764–2776. https://doi.org/10.1063/1.1733103

    Article  CAS  Google Scholar 

  34. Mohammed MH, Williams PA, Tverezovskaya O (2013) Extraction of chitin from prawn shells and conversion to low molecular mass chitosan. Food Hydrocoll 31:166–171. https://doi.org/10.1016/j.foodhyd.2012.10.021

    Article  CAS  Google Scholar 

  35. Mutsenko VV, Bazhenov VV, Rogulska O et al (2017) 3D chitinous scaffolds derived from cultivated marine demosponge Aplysina aerophoba for tissue engineering approaches based on human mesenchymal stromal cells. Int J Biol Macromol 104:1966–1974. https://doi.org/10.1016/j.ijbiomac.2017.03.116

    Article  CAS  PubMed  Google Scholar 

  36. Muzzarelli RAA (2011) Chitin nanostructures in living organisms. Chitin. Springer, Dordrecht, pp 1–34

    Google Scholar 

  37. Nakamura M, Hiratai R, Hentunen T et al (2016) Hydroxyapatite with high carbonate substitutions promotes osteoclast Resorption through osteocyte-like cells. ACS Biomater Sci Eng 2:259–267. https://doi.org/10.1021/acsbiomaterials.5b00509

    Article  CAS  PubMed  Google Scholar 

  38. Okafor N (1965) Isolation of chitin from the shell of the cuttlefish, Sepia officinalis L. Biochim Biophys Acta 101:193–200. https://doi.org/10.1016/0926-6534(65)90050-3

    Article  CAS  PubMed  Google Scholar 

  39. Pandey AR, Singh US, Momin M, Bhavsar C (2017) Chitosan: application in tissue engineering and skin grafting. J Polym Res 24:125. https://doi.org/10.1007/s10965-017-1286-4

    Article  CAS  Google Scholar 

  40. Pangon A, Saesoo S, Saengkrit N et al (2016) Hydroxyapatite-hybridized chitosan/chitin whisker bionanocomposite fibers for bone tissue engineering applications. Carbohydr Polym 144:419–427. https://doi.org/10.1016/j.carbpol.2016.02.053

    Article  CAS  PubMed  Google Scholar 

  41. Paulino AT, Simionato JI, Garcia JC, Nozaki J (2006) Characterization of chitosan and chitin produced from silkworm crysalides. Carbohydr Polym 64:98–103. https://doi.org/10.1016/j.carbpol.2005.10.032

    Article  CAS  Google Scholar 

  42. Penel G, Pottier EC, Leroy G (2003) Raman investigation of calcium carbonate bone substitutes and related biomaterials. Bull Group Int Rech Sci Stomatol Odontol 45:56–59

    CAS  PubMed  Google Scholar 

  43. Pires CTGVMT, Vilela JAP, Airoldi C (2014) The effect of chitin alkaline Deacetylation at different condition on particle properties. Procedia Chem 9:220–225. https://doi.org/10.1016/j.proche.2014.05.026

    Article  CAS  Google Scholar 

  44. Quimque MTJ, Acas MIS (2015) Structural and morphological analyses of chitin and its complex upon manganese ion adsorption. Procedia Chem 16:578–585. https://doi.org/10.1016/j.proche.2015.12.095

    Article  CAS  Google Scholar 

  45. Rinaudo M (2006) Chitin and chitosan: properties and applications. Prog Polym Sci 31:603–632. https://doi.org/10.1016/j.progpolymsci.2006.06.001

    Article  CAS  Google Scholar 

  46. Sagar N, Khanna K, Sardesai VS et al (2016) Bioconductive 3D nano-composite constructs with tunable elasticity to initiate stem cell growth and induce bone mineralization. Mater Sci Eng C 69:700–714. https://doi.org/10.1016/j.msec.2016.07.063

    Article  CAS  Google Scholar 

  47. Shah R, Saha N, Kitano T, Saha P (2014) Preparation of CaCO3-based biomineralized polyvinylpyrrolidone–carboxymethylcellulose hydrogels and their viscoelastic behavior. J Appl Polym Sci 131:40237. https://doi.org/10.1002/app.40237

    Article  CAS  Google Scholar 

  48. Shah R, Saha N, Kuceková Z et al (2016) Properties of biomineralized (CaCO3) PVP-CMC hydrogel with reference to its cytotoxicity. Int J Polym Mater Po 65:619–628. https://doi.org/10.1080/00914037.2016.1157793

    Article  CAS  Google Scholar 

  49. Shen VK, Siderus DW, Krekelberg WP, Hatch HW (2016) Standard reference simulation website, NIST standard reference database. National Institute of Standards and Technology, Gaithersburg MD

    Google Scholar 

  50. Sum Chow K, Khor E, Chwee Aun Wan A (2001) Porous chitin matrices for tissue engineering: fabrication and in vitro cytotoxic assessment. J Polym Res 8:27–35. https://doi.org/10.1007/s10965-006-0132-x

    Article  Google Scholar 

  51. Tolaimate A, Desbrieres J, Rhazi M, Alagui A (2003) Contribution to the preparation of chitins and chitosans with controlled physico-chemical properties. Polymer 44:7939–7952. https://doi.org/10.1016/j.polymer.2003.10.025

    Article  CAS  Google Scholar 

  52. Tortet L, Gavarri JR, Nihoul G, Dianoux AJ (1997) Study of Protonic mobility in CaHPO4·2H2O (Brushite) and CaHPO4(Monetite) by infrared spectroscopy and neutron scattering. J Solid State Chem 132:6–16. https://doi.org/10.1006/jssc.1997.7383

    Article  CAS  Google Scholar 

  53. Treenate P, Monvisade P, Yamaguchi M (2014) Development of hydroxyethylacryl chitosan/alginate hydrogel films for biomedical application. J Polym Res 21:601. https://doi.org/10.1007/s10965-014-0601-6

    Article  CAS  Google Scholar 

  54. Vittori M, Srot V, Žagar K et al (2016) Axially aligned organic fibers and amorphous calcium phosphate form the claws of a terrestrial isopod (Crustacea). J Struct Biol 195:227–237. https://doi.org/10.1016/j.jsb.2016.06.008

    Article  CAS  PubMed  Google Scholar 

  55. Walther LE, Blödow A, Buder J, Kniep R (2014) Principles of calcite dissolution in human and artificial Otoconia. PLoS One 9:e102516. https://doi.org/10.1371/journal.pone.0102516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Younes I, Rinaudo M (2015) Chitin and chitosan preparation from marine sources. Structure, properties and applications. Mar Drugs 13:1133–1174. https://doi.org/10.3390/md13031133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The assistance of Galja Pletikapić, PhD. in AFM measurements is highly appreciated, as is that of Ayan Ray, PhD. for simple compression measurements. This work has been supported by the Croatian Science Foundation under project IP-2013-11-5055 and the Ministry of Education, Youth and Sports of the Czech Republic, Program NPU I (LO1504). The work was performed according to the work plan of COST Action MP1301, New Generation Biomimetic, and Customized Implants for Bone Engineering “NEWGEN”. The first author is thankful to COST Action MP1301 for providing financial support in the framework of its 5th call for STSM 2016.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Vida Čadež or Nabanita Saha.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Čadež, V., Šegota, S., Sondi, I. et al. Calcium phosphate and calcium carbonate mineralization of bioinspired hydrogels based on β-chitin isolated from biomineral of the common cuttlefish (Sepia officinalis, L.). J Polym Res 25, 226 (2018). https://doi.org/10.1007/s10965-018-1626-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10965-018-1626-z

Keywords

Navigation