Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Cell-adhesive gels made of sacran/collagen complexes

Polymer Journal volume 54, pages 581–589 (2022)Cite this article

Subjects

Abstract

Anionic polysaccharides (“sacran”) are expected to be useful as medical materials, such as cell cultivation scaffolds. In this study, polymer complex gels of sacran with cell-compatible proteins and collagen were prepared. Complex gels of sacran and collagen were observed using fluorescence and polarized microscopes, which indicated the complexation characteristics of sacran and collagen, as well as their partial orientation. Infrared spectroscopy revealed the gel formation of the polymer complexes. The addition of NaCl was observed to control the uniformity of the complex gels, which suggests that the main interaction in the complexation of anionic sacran with cationic functional groups of collagens is ionic. The swelling degree of the complex gel was significantly lower than that of the sacran-only gel, and the degree of cell adhesion of the complex gel was as high as that on tissue culture-treated polystyrene (positive control); this indicates that the introduction of collagen into sacran gels is effective for cell cultivation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev. 2016;97:4–27.

    Article  CAS  PubMed  Google Scholar 

  2. Bosman FT, Stamenkovic I. Functional structure and composition of the extracellular matrix. J Pathol. 2003;200:423–8.

    Article  CAS  PubMed  Google Scholar 

  3. Dubiel EA, Martin Y, Vermette P. Bridging the gap between physicochemistry and interpretation prevalent in cell–surface interactions. Chem Rev. 2011;111:2900–36.

    Article  CAS  PubMed  Google Scholar 

  4. Delair T. In situ forming polysaccharide-based 3D-hydrogels for cell delivery in regenerative medicine. Carbohydr Polym. 2012;87:1013–9.

    Article  CAS  Google Scholar 

  5. Hong Y, Gong Y, Gao C, Shen J. Collagen-coated polylactide microcarriers/chitosan hydrogel composite: Injectable scaffold for cartilage regeneration. J Biomed Mater Res A. 2008;85A:628–37.

    Article  CAS  Google Scholar 

  6. Lau TT, Wang C, Png SW, Su K, Wang D-A. Genipin-crosslinked microcarriers mediating hepatocellular aggregates formation and functionalities. J Biomed Mater Res A. 2011;96A:204–11.

    Article  CAS  Google Scholar 

  7. Picheth GF, Pirich CL, Sierakowski MR, Woehl MA, Sakakibara CN, de Souza CF, et al. Bacterial cellulose in biomedical applications: a review. Int J Biol Macromolecules. 2017;104:97–106.

    Article  CAS  Google Scholar 

  8. Okeyoshi K, Okajima MK, Kaneko T. The cyanobacterial polysaccharide sacran: characteristics, structures, and preparation of LC gels. Polym J. 2021;53:81–91.

    Article  CAS  Google Scholar 

  9. Ngatu NR, Okajima MK, Yokogawa M, Hirota R, Eitoku M, Muzembo BA, et al. Anti-inflammatory effects of sacran, a novel polysaccharide from Aphanothece sacrum, on 2,4,6-trinitrochlorobenzene–induced allergic dermatitis in vivo. Ann Allergy Asthma Immunol. 2012;108:117–22.e2.

    Article  CAS  PubMed  Google Scholar 

  10. Puluhulawa LE, Joni IM, Mohammed AFA, Arima H, Wathoni N. The use of megamolecular polysaccharide sacran in food and biomedical applications. Molecules. 2021;26:3362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Okajima MK, Higashi T, Asakawa R, Mitsumata T, Kaneko D, Kaneko T, et al. Gelation behavior by the lanthanoid adsorption of the cyanobacterial extracellular polysaccharide. Biomacromolecules. 2010;11:3172–7.

    Article  CAS  PubMed  Google Scholar 

  12. Okajima MK, Nakamura M, Mitsumata T, Kaneko T. Cyanobacterial polysaccharide gels with efficient rare-earth-metal sorption. Biomacromolecules. 2010;11:1773–8.

    Article  CAS  PubMed  Google Scholar 

  13. Shikinaka K, Okeyoshi K, Masunaga H, Okajima MK, Kaneko T. Solution structure of cyanobacterial polysaccharide, sacran. Polymer. 2016;99:767–70.

    Article  CAS  Google Scholar 

  14. Goto M, Azuma K, Arima H, Kaneko S, Higashi T, Motoyama K, et al. Sacran, a sulfated polysaccharide, suppresses the absorption of lipids and modulates the intestinal flora in non-alcoholic steatohepatitis model rats. Life Sci. 2021;268:118991.

    Article  CAS  PubMed  Google Scholar 

  15. Motoyama K, Tanida Y, Hata K, Hayashi T, Higashi T, Ishitsuka Y, et al. Potential use of a megamolecular polysaccharide sacran as a hydrogel-based sustained release system. Chem Pharm Bull. 2014;62:636–41.

    Article  CAS  Google Scholar 

  16. Joshi G, Okeyoshi K, Okajima MK, Kaneko T. Directional control of diffusion and swelling in megamolecular polysaccharide hydrogels. Soft Matter. 2016;12:5515–8.

    Article  CAS  PubMed  Google Scholar 

  17. Okeyoshi K, Okajima MK, Kaneko T. Milliscale self-integration of megamolecule biopolymers on a drying gas–aqueous liquid crystalline interface. Biomacromolecules. 2016;17:2096–103.

    Article  CAS  PubMed  Google Scholar 

  18. Okeyoshi K, Joshi G, Rawat S, Sornkamnerd S, Amornwachirabodee K, Okajima MK, et al. Drying-induced self-similar assembly of megamolecular polysaccharides through nano and submicron layering. Langmuir. 2017;33:4954–9.

    Article  CAS  PubMed  Google Scholar 

  19. Okajima MK, Mishima R, Amornwachirabodee K, Mitsumata T, Okeyoshi K, Kaneko T. Anisotropic swelling in hydrogels formed by cooperatively aligned megamolecules. RSC Adv. 2015;5:86723–9.

    Article  CAS  Google Scholar 

  20. Bunyaratavej P, Wang H-L. Collagen membranes: a review. J Periodontol. 2001;72:215–29.

    Article  CAS  PubMed  Google Scholar 

  21. Visser R, Arrabal PM, Santos-Ruiz L, Fernandez-Barranco R, Becerra J, Cifuentes M. A collagen-targeted biomimetic RGD peptide to promote osteogenesis. Tissue Eng A. 2013;20:34–44.

    Article  Google Scholar 

  22. Burgess BT, Myles JL, Dickinson RB. Quantitative analysis of adhesion-mediated cell migration in three-dimensional gels of RGD-grafted collagen. Ann Biomed Eng. 2000;28:110–8.

    Article  CAS  PubMed  Google Scholar 

  23. Yamada S, Yamamoto K, Ikeda T, Yanagiguchi K, Hayashi Y. Potency of fish collagen as a scaffold for regenerative medicine. BioMed Res Int. 2014;2014:302932.

  24. Smith JW. Molecular pattern in native collagen. Nature. 1968;219:157–8.

    Article  CAS  PubMed  Google Scholar 

  25. Nomura S, Hiltner A, Lando JB, Baer E. Interaction of water with native collagen. Biopolymers. 1977;16:231–46.

    Article  CAS  PubMed  Google Scholar 

  26. Park J-C, Hwang Y-S, Lee J-E, Park KD, Matsumura K, Hyon S-H, et al. Type I atelocollagen grafting onto ozone-treated polyurethane films: Cell attachment, proliferation, and collagen synthesis. J Biomed Mater Res. 2000;52:669–77.

    Article  CAS  PubMed  Google Scholar 

  27. DeLustro F, Condell RA, Nguyen MA, McPherson JM. A comparative study of the biologic and immunologic response to medical devices derived from dermal collagen. J Biomed Mater Res. 1986;20:109–20.

    Article  CAS  PubMed  Google Scholar 

  28. Wood GC. The formation of fibrils from collagen solutions. 2. A mechanism of collagen-fibril formation. Biochem J. 1960;75:598–605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rosenblatt J, Devereux B, Wallace DG. Injectable collagen as a pH-sensitive hydrogel. Biomaterials. 1994;15:985–95.

    Article  CAS  PubMed  Google Scholar 

  30. Silver FH, Freeman JW, Seehra GP. Collagen self-assembly and the development of tendon mechanical properties. J Biomech. 2003;36:1529–53.

    Article  PubMed  Google Scholar 

  31. Achilli M, Mantovani D. Tailoring mechanical properties of collagen-based scaffolds for vascular tissue engineering: the effects of pH, temperature and ionic strength on gelation. Polymers. 2010;2:664–80.

    Article  CAS  Google Scholar 

  32. Yang Y-l, Kaufman LJ. Rheology and confocal reflectance microscopy as probes of mechanical properties and structure during collagen and collagen/hyaluronan self-assembly. Biophysical J. 2009;96:1566–85.

    Article  CAS  Google Scholar 

  33. Yu X, Yuan Q, Yang M, Liu R, Zhu S, Li J, et al. Development of biocompatible and antibacterial collagen hydrogels via dialdehyde polysaccharide modification and tetracycline hydrochloride loading. Macromol Mater Eng. 2019;304:1800755.

    Article  Google Scholar 

  34. Norris K, Mishukova OI, Zykwinska A, Colliec-Jouault S, Sinquin C, Koptioug A, et al. Marine polysaccharide-collagen coatings on Ti6Al4V alloy formed by self-assembly. Micromachines. 2019;10:68.

    Article  PubMed Central  Google Scholar 

  35. Xu J, Zheng S, Hu X, Li L, Li W, Parungao R, et al. Advances in the research of bioinks based on natural collagen, polysaccharide and their derivatives for skin 3D bioprinting. Polymers. 2020;12:1237.

    Article  CAS  PubMed Central  Google Scholar 

  36. Okajima MK, Bamba T, Kaneso Y, Hirata K, Fukusaki E, Kajiyama SI, et al. Supergiant ampholytic sugar chains with imbalanced charge ratio form saline ultra-absorbent hydrogels. Macromolecules. 2008;41:4061–4.

    Article  CAS  Google Scholar 

  37. Omidian H, Hashemi SA, Sammes PG, Meldrum I. A model for the swelling of superabsorbent polymers. Polymer. 1998;39:6697–704.

    Article  CAS  Google Scholar 

  38. Raju MP, Raju KM. Design and synthesis of superabsorbent polymers. J Appl Polym Sci. 2001;80:2635–9.

    Article  CAS  Google Scholar 

  39. Ross AM, Jiang Z, Bastmeyer M, Lahann J. Physical aspects of cell culture substrates: topography, roughness, and elasticity. Small. 2012;8:336–55.

    Article  CAS  PubMed  Google Scholar 

  40. Okajima-Kaneko M, Ono M, Kabata K, Kaneko T. Extraction of novel sulfated polysaccharides from Aphanothece sacrum (Sur.) Okada, and its spectroscopic characterization. Pure Appl Chem. 2007;79:2039–46.

    Article  CAS  Google Scholar 

  41. Amornwachirabodee K, Okajima MK, Kaneko T. Uniaxial swelling in LC hydrogels formed by two-step cross-linking. Macromolecules. 2015;48:8615–21.

    Article  CAS  Google Scholar 

  42. Tsutsumi S, Shimazu A, Miyazaki K, Pan H, Koike C, Yoshida E, et al. Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun. 2001;288:413–9.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Shibuya Science and Sports Culture Foundation and partially supported by a Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Early-Career Scientists (21K14681) and the A-step (AS2915173U) of the Japan Science and Technology Agency (JST), Japan.

Author information

Authors and Affiliations

  1. Graduate School of Advanced Science and Technology, Japan Advanced Institute of Science and Technology, Nomi, Ishikawa, Japan

    Kenji Takada, Asuka Komuro, Mohammad Asif Ali, Maninder Singh, Maiko Okajima, Kazuaki Matsumura & Tatsuo Kaneko

  2. Soft Matter Sciences and Engineering Laboratory, ESPCI Paris, PSL University, CNRS, Paris, France

    Mohammad Asif Ali

Authors
  1. Kenji Takada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Asuka Komuro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Asif Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maninder Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maiko Okajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kazuaki Matsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tatsuo Kaneko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tatsuo Kaneko.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takada, K., Komuro, A., Ali, M.A. et al. Cell-adhesive gels made of sacran/collagen complexes. Polym J 54, 581–589 (2022). https://doi.org/10.1038/s41428-021-00593-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41428-021-00593-w

This article is cited by

Search

Advanced search

Quick links