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Incorporation of Collagen from Marine Sponges (Spongin) into Hydroxyapatite Samples: Characterization and In Vitro Biological Evaluation

  • J. R. Parisi
  • K. R. Fernandes
  • I. R. Avanzi
  • B. P. Dorileo
  • A. F. Santana
  • A. L. Andrade
  • P. R. Gabbai-Armelin
  • C. A. Fortulan
  • E. S. Trichês
  • R. N. Granito
  • A. C. M. Renno
Original Article
  • 22 Downloads

Abstract

Biomaterial-based bone grafts have an important role in the field of bone tissue engineering. One of the most promising classes of biomaterials is collagen, including the ones from marine biodiversity (in general, called spongin (SPG)). Also, hydroxyapatite (HA) has an important role in stimulating bone metabolism. Therefore, this work investigated the association of HA and SPG composites in order to evaluate their physico-chemical and morphological characteristics and their in vitro biological performance. For this, pre-set composite disks were evaluated by means of mass loss after incubation, pH, Fourier transform infrared spectroscopy (FTIR), scanning electron microscopy (SEM), and “in vitro” cell viability. pH measurements showed no statistical difference between groups. Moreover, a higher mass loss was observed for HA/SPG70/30 compared to the other groups for all experimental periods. Moreover, SEM representative micrographs showed the degradation of the samples with and without immersion. FTIR analysis demonstrated the absorption peaks for poly(methyl methacrylate) (PMMA), HA, and SPG. A higher L292 cell viability for control and PMMA was observed compared to HA and HA/SPG 90/10. Also, HA/SPG 70/30 showed higher cell viability compared to HA and HA/SPG 90/10 on days 3 and 7 days of culture. Furthermore, HA showed a significant lower MC3T3 cell viability compared to control and HA/SPG 70/30 on day 3 and no significant difference was observed between the composites in the last experimental period. Based on our investigations, it can be concluded that the mentioned composites were successfully obtained, presenting improved biological properties, especially the one mimicking the composition of bone (with 70% of HA and 30% of SPG). Consequently, these data highlight the potential of the introduction of SPG into HA to improve the performance of the graft for bone regeneration applications. Further long-term studies should be carried out to provide additional information concerning the late stages of material degradation and bone healing in the presence of HA/SPG.

Keywords

Collagen Marine biotechnology Marine biomaterials Tissue engineering Biomedical application 

Notes

Acknowledgments

The authors would like to acknowledge CAPES Foundation, Ministry of Education of Brazil, Brasilia-DF, Brazil. Prof. Dr. Márcio Reis Custódio from Department of General Physiology of the Institute of Biosciences (IB-USP) for the assistance with this experiment.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Amini AR, Laurencin CT, Nukavarapu SP (2012) Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng 40:363–408CrossRefPubMedPubMedCentralGoogle Scholar
  2. Berzina-Cimdina L, Borodajenko N (2012) Research of calcium phosphates using Fourier transform infrared spectroscopy. In: Theophile T (ed) Infrared spectroscopy - materials science, engineering and technology. InTech. Available from: http://www.intechopen.com/books/infrared-spectroscopy-materials-science-engineeringandtechnology/research-of-calcium-phosphates-using-fourier-transformation-infrared-spectroscopy. Accessed 11 Sept 2018Google Scholar
  3. Bijlsma JW, Berenbaum F, Lafeber FP (2011) Osteoarthritis: an update with relevance for clinical practice. Lancet 18:2115–2126CrossRefGoogle Scholar
  4. Black CRM, Goriainov V, Gibbs D, Kanczler J, Tare RS, Oreffo ROC (2015) Bone tissue engineering. Curr Mol Biol Rep 3:132–140CrossRefGoogle Scholar
  5. Bose S, Roy M, Bandyopadhyay A (2015) Recent advances in bone tissue engineering scaffolds. Trends Biotechnol 30:546–554CrossRefGoogle Scholar
  6. Duan G, Zhang C, Li A, Yang X, Lu L, Wang X (2008) Preparation and characterization of mesoporous zirconia made by using a poly (methyl methacrylate) template. Nanoscale Res Lett 3:118–122CrossRefPubMedPubMedCentralGoogle Scholar
  7. Einhorn TA, Gerstenfeld LC (2015) Fracture healing: mechanisms and interventions. Nat Rev Rheumatol 11:45–54CrossRefGoogle Scholar
  8. Exposito JY, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268:302–316CrossRefPubMedGoogle Scholar
  9. Granito RN, Custódio MR, Rennó AC (2017) Natural marine sponges for bone tissue engineering: the state of art and future perspectives. J Biomed Mater Res B Appl Biomater 105:1717–1727CrossRefPubMedGoogle Scholar
  10. Green D, Howard D, Yang X, Kelly M, Oreffo RO (2003) Natural marine sponge fiber skeleton: a biomimetic scaffold for human osteoprogenitor cell attachment, growth, and differentiation. Tissue Eng 9:1159–1166CrossRefPubMedGoogle Scholar
  11. Haach LCA (2015) Corpos compósitos de poli(metacrilato de metila) com microfibra de biovidro e poros para reparo de defeitos ósseos. Universidade de Sao Paulo, Sao CarlosCrossRefGoogle Scholar
  12. Habibovic P, Sees TM, van den Doel MA et al (2006) Osteoinduction by biomaterials - physicochemical and structural influences. J Biomed Mater Res A 774:747–762CrossRefGoogle Scholar
  13. Iwatsubo T, Kishi R, Miura T, Ohzono T, Yamaguchi T (2015) Formation of hydroxyapatite skeletal materials from hydrogel matrices via artificial biomineralization. J Phys Chem B 119:8793–8799CrossRefPubMedGoogle Scholar
  14. Kwak HB (2013) Aging, exercise, and extracellular matrix in the heart. J Exerc Rehabil 9:338–347CrossRefPubMedPubMedCentralGoogle Scholar
  15. Laurenti KC, Haach LCA, ARd SJ et al (2014) Cartilage reconstruction using self-anchoring implant with functional gradient. Mater Res 17:638–649CrossRefGoogle Scholar
  16. Lim HK, Byun SH, Woo JM, Kim SM, Lee SM, Kim BJ, Kim HE, Lee JW, Kim SM, Lee JH (2017) Biocompatibility and biocorrosion of hydroxyapatite-coated magnesium plate: animal experiment. Materials 10:1149CrossRefPubMedCentralGoogle Scholar
  17. Lin Z, Solomon KL, Zhang X, Pavlos NJ, Abel T, Willers C, Dai K, Xu J, Zheng Q, Zheng M (2011) In vitro evaluation of natural marine sponge collagen as a scaffold for bone tissue engineering. Int J Biol Sci 7:968–977CrossRefPubMedPubMedCentralGoogle Scholar
  18. Lobo AO, Zanin H, Siqueira IA, Leite NC, Marciano FR, Corat EJ (2013) Effect of ultrasound irradiation on the production of nHAp/MWCNT nanocomposites. Mater Sci Eng C Mater Biol Appl 33:4305–4312CrossRefPubMedGoogle Scholar
  19. Lopez-Heredia MA, Sa Y, Salmon P, de Wijn JR, Wolke JG, Jansen JA (2012) Bulk properties and bioactivity assessment of porous polymethylmethacrylate cement loaded with calcium phosphates under simulated physiological conditions. Acta Biomater 8:3120–3127CrossRefPubMedGoogle Scholar
  20. Lu HH, El-Amin SF, Scott KD et al (2003) Three-dimensional, bioactive, biodegradable, polymer-bioactive glass composite scaffolds with improved mechanical properties support collagen synthesis and mineralization of human osteoblast-like cells in vitro. J Biomed Mater Res A 64:465–474CrossRefPubMedGoogle Scholar
  21. Lu HH, Tang A, Oh SC, Spalazzi JP, Dionisio K (2005) Compositional effects on the formation of a calcium phosphate layer and the response of osteoblast-like cells on polymer-bioactive glass composites. Biomaterials 32:6323–6334CrossRefGoogle Scholar
  22. Magri AMP, Fernandes KR, Ueno FR, Kido HW, Da Silva AC, Braga FJC, Granito RN, Gabbai-Armelin PR, Rennó ACM (2017) Osteoconductive properties of two different bioactive glass forms (powder and fiber) combined with collagen. Appl Surf Sci 423:557–565CrossRefGoogle Scholar
  23. Nuss KMR, von Rechenberg B (2008) Biocompatibility issues with modern implants in bone - a review for clinical orthopedics. Open Orthop J 2:66–78CrossRefPubMedPubMedCentralGoogle Scholar
  24. Oryan A, Baghaban Eslaminejad M, Kamali A, Hosseini S, Sayahpour FA, Baharvand H (2018) Synergistic effect of strontium, bioactive glass and nano-hydroxyapatite promotes bone regeneration of critical-sized radial bone defects. J Biomed Mater Res B Appl Biomater.  https://doi.org/10.1002/jbm.b.34094
  25. Ozel T, Bártolo PJ, Ceretti E, De Ciurana Gay J, Rodriguez CA, Da Silva JVL (2016) Biomedical devices: design, prototyping, and manufacturing. John Wiley & Sons, New JerseyGoogle Scholar
  26. Pang KM, Lee JK, Seo YK, Kim SM, Kim MJ, Lee JH (2015) Biologic properties ofnano-hydroxyapatite: an in vivo study of calvarial defects, ectopic bone formation and bone implantation. Biomed Mater Eng 25:25–38PubMedGoogle Scholar
  27. Parizi AM, Oryan A, Shafiei-Sarvestani Z, Bigham-Sadegh A (2013) Effectiveness of synthetic hydroxyapatite versus Persian Gulf coral in an animal model of long bone defect reconstruction. J Orthop Traumatol 14:259–268CrossRefPubMedPubMedCentralGoogle Scholar
  28. Qi X, Ye J, Wang Y (2008) Improved injectability and in vitro degradation of a calcium phosphate cement containing poly(lactide-co-glycolide) microspheres. Acta Biomater 4:1837–1845CrossRefPubMedGoogle Scholar
  29. Ramírez-Rodríguez GB, Delgado-López JM, Iafisco M, Montesi M, Sandri M, Sprio S, Tampieri A (2016) Biomimetic mineralization of recombinant collagen type I derived protein to obtain hybrid matrices for bone regeneration. J Struct Biol 196:138–146CrossRefPubMedGoogle Scholar
  30. Rizwan M, Hamdi M, Basirun WJ (2017) Bioglass® 45S5-based composites for bone tissue engineering and functional applications. J Biomed Mater Res A 105:3197–3223CrossRefPubMedGoogle Scholar
  31. Ruhé P, Hedberg E, Padron NT, Spauwen PH, Jansen JA, Mikos AG (2005) Biocompatibility and degradation of poly(DL-lactic-co-glycolic acid)/calcium phosphate cement composites. J Biomed Mater Res A 74:533–544CrossRefPubMedGoogle Scholar
  32. Scarano A, Lorusso F, Staiti G, Sinjari B, Tampieri A, Mortellaro C (2017) Sinus augmentation with biomimetic nanostructured matrix: tomographic, radiological, histological and histomorphometrical results after 6 months in humans. Front Physiol 8:565CrossRefPubMedPubMedCentralGoogle Scholar
  33. Shin H, Quinten Ruhe P, Mikos AG, Jansen JA (2003) In vivo bone and soft tissue response to injectable, biodegradable oligo(poly(ethylene glycol) fumarate) hydrogels. Biomaterials 24:3201–3211CrossRefPubMedGoogle Scholar
  34. Silva TH, Moreira-Silva J, Marques ALP, Domingues A, Bayon Y, Reis RL (2014) Marine origin collagens and its potential applications Ehrlich H, ed. Marine Drugs 12:5881–5901CrossRefPubMedPubMedCentralGoogle Scholar
  35. Sousa THS (2009) Projeto conceitual de implante bioativo com gradiente de estrutura funcional em PMMA e HA. Analises: in vitro e in vivo. Universidade de Sao Paulo, Sao CarlosGoogle Scholar
  36. Swatschek D, Schatton W, Kellermann J, Müller WE, Kreuter J (2002) Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. Eur J Pharm Biopharm 53:107–113CrossRefPubMedGoogle Scholar
  37. Szpalski C, Barr J, Wetterau M, Saadeh PB, Warren SM (2010) Cranial bone defects: current and future strategies. Neurosurg Focus 29:6–8CrossRefGoogle Scholar
  38. Välimäki V-V, Yrjans JJ, Vuorio E, Aro HT (2005) Molecular biological evaluation of adjunct treatment with BMP-2 gene transfer and bioactive glass microspheres in enhancement of new bone formation. Tissue Eng 11:387–394CrossRefPubMedGoogle Scholar
  39. van de Watering FCJ, van den Beucken JJJP, Walboomers XF, Jansen JA (2012) Calcium phosphate/poly(d,l-lactic-co-glycolic acid) composite bone substitute materials: evaluation of temporal degradation and bone ingrowth in a rat critical-sized cranial defect. Clin Oral Implants Res 23:151–159CrossRefPubMedGoogle Scholar
  40. Wang H, Li Y, Zuo Y, Li J, Ma S, Cheng L (2007) Biocompatibility and osteogenesis of biomimetic nano-hydroxyapatite/polyamide composite scaffolds for bone tissue engineering. Biomaterials 28:3338–3348CrossRefGoogle Scholar
  41. Wang B, Dong J, Zhou X, Lee KJ, Huang R, Zhang S, Liu Y (2009) Nucleosides from the marine sponge Haliclona sp. Z Naturforsch C 64:143–148CrossRefPubMedGoogle Scholar
  42. Wang L, Yoon DM, Spicer PP, Henslee AM, Scott DW, Wong ME et al (2013) Characterization of porous polymethylmethacrylate space maintainers for craniofacial reconstruction. J Biomed Mater Res B Appl Biomater 101:813–825CrossRefPubMedGoogle Scholar
  43. Zdarta J, Norman M, Smułek W, Moszyński D, Kaczorek E, Stelling A, Ehrlich H, Jesionowski T (2017) Spongin-based scaffolds from Hippospongia communis demosponge as an effective support for lipase immobilization. Catalysts 7:147CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • J. R. Parisi
    • 1
  • K. R. Fernandes
    • 1
  • I. R. Avanzi
    • 2
  • B. P. Dorileo
    • 2
  • A. F. Santana
    • 2
  • A. L. Andrade
    • 1
  • P. R. Gabbai-Armelin
    • 2
  • C. A. Fortulan
    • 3
  • E. S. Trichês
    • 4
  • R. N. Granito
    • 2
  • A. C. M. Renno
    • 2
  1. 1.Department of PhysiotherapyFederal University of São Carlos (UFSCar)São CarlosBrazil
  2. 2.Department of BiosciencesFederal University of São Paulo (UNIFESP)SantosBrazil
  3. 3.Department of Mechanical EngineeringSão Carlos School of Engineering São CarlosSão CarlosBrazil
  4. 4.Department of Mechanical EngineeringFederal University of São Paulo (UNIFESP)São José dos CamposBrazil

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