Advertisement

Marine Derived Biomaterials for Bone Regeneration and Tissue Engineering: Learning from Nature

  • Besim Ben-NissanEmail author
  • Andy H. Choi
  • David W. Green
Chapter
Part of the Springer Series in Biomaterials Science and Engineering book series (SSBSE, volume 14)

Abstract

Marine structures, biogenic materials, and biomimetic approaches applied to the fabrication of advanced biomaterials and implants are used to address the shortcomings of existing scaffold designs that are biologically un-responsive throughout the regeneration process and lack necessary versatility. Bioactive ceramics converted from biostructures or natural marine-based materials such as corals, sea urchin, sponges and shells are being designed into functional scaffolds that can adapt and evolve to changing environment during regeneration process. They can regulate cell responses at nanostructured surfaces, and as modules for self-assembling by the patient’s own cells and as smart devices that possess tissue specific homing capabilities. These natural structures can be converted to bioactive ceramics such as hydroxyapatite to assist osseointegration. This chapter covers biomimicry, evolution of marine structures, and their specific use and current research on natural materials such as coral, sponge, sea urchin, sponge nacre, and foraminifera as models and raw materials for bioactive bone scaffolding materials and tissue engineering.

Keywords

Marine structures Hydroxyapatite Bioactive Biogenic Biomimetics Coral Nacre Bone grafts Scaffolding 

Notes

Acknowledgements

I would like to sincerely thank Dr. David W. Green, Dr. Innocent Macha, Dr. Jimmy Hu, Prof. Faik Oktar and Associate Profs. Sophie Cazelbou and Sibel Akyol and a large number of our students and postdocs that contributed to research in marine materials and their application in the medical field.

References

  1. 1.
    Bielby RC, Boccaccini AR, Polak JM et al (2004) In vitro differentiation and in vivo mineralization of osteogenic cells derived from human embryonic stem cells. Tissue Eng 10:1518–1525Google Scholar
  2. 2.
    Vincent JF, Bogatyreva OA, Bogatyrev NR et al (2006) Biomimetics: its practice and theory. J R Soc Interface 3:471–482Google Scholar
  3. 3.
    Collier JH (2008) Modular self-assembling biomaterials for directing cellular responses. Soft Matter 4:2310–2315Google Scholar
  4. 4.
    Polak JM, Bishop AE (2006) Stem cells and tissue engineering: past, present, and future. Ann N Y Acad Sci 1068:352–366Google Scholar
  5. 5.
    Chau Y, Luo Y, Cheung AC et al (2008) Incorporation of a matrix metalloproteinase-sensitive substrate into self-assembling peptides—a model for biofunctional scaffolds. Biomaterials 29:1713–1719Google Scholar
  6. 6.
    Green DW, Lai WF, Jung HS (2014) Evolving marine biomimetics for regenerative dentistry. Mar Drugs 12:2877–2912Google Scholar
  7. 7.
    Chung BG, Kang L, Khademhosseini A (2007) Micro- and nanoscale technologies for tissue engineering and drug discovery applications. Expert Opin Drug Discov 2:1653–1668Google Scholar
  8. 8.
    Khademhosseini A, Ling Y, Karp JM et al (2007) Micro- and nanoscale control of cellular environment for tissue engineering. In: Mirkin CA, Niemeyer CM (eds) Nanobiotechnology II: more concepts and applications. Wiley, New York, pp 347–364Google Scholar
  9. 9.
    Chen ZC, Ekaputra AK, Gauthaman K et al (2008) In vitro and in vivo analysis of co-electrospun scaffolds made of medical grade poly(epsilon-caprolactone) and porcine collagen. J Biomater Sci Polym Ed 19:693–707Google Scholar
  10. 10.
    Ben-Nissan B (2015) Discovery and development of marine biomaterials. In: Kim SK (ed) Functional marine biomaterials, properties and applications. Woodhead Publishing, Cambridge, pp 3–32Google Scholar
  11. 11.
    Macha IJ, Ben-Nissan B (2018) Marine skeletons: towards hard tissue repair and regeneration. Mar Drugs 16:E225.  https://doi.org/10.3390/md16070225Google Scholar
  12. 12.
    Green D, Walsh D, Mann S et al (2002) The potential of biomimesis in bone tissue engineering: lessons from the design and synthesis of invertebrate skeletons. Bone 30:810–815Google Scholar
  13. 13.
    Green D, Walsh D, Yang X et al (2004) Stimulation of human bone marrow stromal cells using growth factor encapsulated calcium carbonate porous microspheres. J Mater Chem 14:2206–2212Google Scholar
  14. 14.
    Fujita N, Asai M, Yamashita T et al (2004) Sol–gel transcription of silica-based hybrid nanostructures using poly(N-vinylpyrrolidone)-coated [60]fullerene, single-walled carbon nanotube and block copolymer templates. J Mater Chem 14:2106–2114Google Scholar
  15. 15.
    Rautaray D, Ahmad A, Sastry M (2004) Biological synthesis of metal carbonate minerals using fungi and actinomycetes. J Mater Chem 14:2333–2340Google Scholar
  16. 16.
    Kulp JL III, Sarikaya M, Evans JS (2004) Molecular characterization of a prokaryotic polypeptide sequence that catalyzes Au crystal formation. J Mater Chem 14:2325–2332Google Scholar
  17. 17.
    Ben-Nissan B (2003) Natural bioceramics: from coral to bone and beyond. Curr Opin Solid State Mater Sci 7:283–288Google Scholar
  18. 18.
    Mann S (1993) Molecular tectonics in biomineralization and biomimetic materials chemistry. Nature 365:499–505Google Scholar
  19. 19.
    Mann S, Ozin GA (1996) Synthesis of inorganic materials with complex form. Nature 382:313–318Google Scholar
  20. 20.
    Green DW, Padula MP, Santos J et al (2013) A therapeutic potential for marine skeletal proteins in bone regeneration. Mar Drugs 11:1203–1220Google Scholar
  21. 21.
    Petite H, Viateau V, Bensaïd W et al (2000) Tissue-engineered bone regeneration. Nat Biotechnol 18:959–963Google Scholar
  22. 22.
    Leupold JA, Barfield WR, An YH et al (2006) A comparison of ProOsteon, DBX, and collagraft in a rabbit model. J Biomed Mater Res B Appl Biomater 79:292–297Google Scholar
  23. 23.
    Abramovitch-Gottlib L, Geresh S, Vago R (2006) Biofabricated marine hydrozoan: a bioactive crystalline material promoting ossification of mesenchymal stem cells. Tissue Eng 12:729–739Google Scholar
  24. 24.
    Green DW, Ben-Nissan B (2015) Biomimetic applications in regenerative medicine: scaffolds, transplantation modules, tissue homing devices, and stem cells. In: Bawa R, Audette G, Rubinstein I (eds) Handbook of clinical nanomedicine: nanoparticles, imaging, therapy, and clinical applications. Pan Stanford Publishing, Singapore, pp 1109–1140Google Scholar
  25. 25.
    Parker AR, Townley HE (2007) Biomimetics of photonic nanostructures. Nat Nanotechnol 2:347–353Google Scholar
  26. 26.
    Kim ES (2008) Directed evolution: a historical exploration into an evolutionary experimental system of nanobiotechnology, 1965–2006. Minerva 46:463–484Google Scholar
  27. 27.
    Marga F, Neagu A, Kosztin I et al (2007) Developmental biology and tissue engineering. Birth Defects Res C Embryo Today 81:320–328Google Scholar
  28. 28.
    Sia SK, Gillette BM, Yang GJ (2007) Synthetic tissue biology: tissue engineering meets synthetic biology. Birth Defects Res C Embryo Today 81:354–361Google Scholar
  29. 29.
    Andrianantoandro E, Basu S, Karig DK et al (2006) Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2(2006):0028Google Scholar
  30. 30.
    Ingber DE (1998) The architecture of life. Sci Am 278:48–57Google Scholar
  31. 31.
    Hu J, Fraser R, Russell JJ et al (2000) Australian coral as a biomaterial: characteristics. J Mater Sci Technol 16:591–595Google Scholar
  32. 32.
    Hu J, Russell JJ, Ben-Nissan B et al (2001) Production and analysis of hydroxyapatite from Australian corals via hydrothermal process. J Mater Sci Lett 20:85–87Google Scholar
  33. 33.
    Rocha JH, Lemos AF, Agathopoulos S et al (2005) Scaffolds for bone restoration from cuttlefish. Bone 37:850–857Google Scholar
  34. 34.
    Green D, Howard D, Yang X et al (2003) Natural marine sponge fiber skeleton: a biomimetic scaffold for human osteoprogenitor cell attachment, growth, and differentiation. Tissue Eng 9:1159–1166Google Scholar
  35. 35.
    Martina M, Subramanyam G, Weaver JC et al (2005) Developing macroporous bicontinuous materials as scaffolds for tissue engineering. Biomaterials 26:5609–5616Google Scholar
  36. 36.
    Townley H, Parker A, White-Cooper H (2008) Exploitation of diatom frustules for nanotechnology: tethering active biomolecules. Adv Funct Mater 18:369–374Google Scholar
  37. 37.
    Marin F, Luquet G, Marie B et al (2007) Molluscan shell proteins: primary structure, origin, and evolution. Curr Top Dev Biol 80:209–276Google Scholar
  38. 38.
    Rocha JH, Lemos AF, Agathopoulos S et al (2006) Hydrothermal growth of hydroxyapatite scaffolds from aragonitic cuttlefish bones. J Biomed Mater Res A 77:160–168Google Scholar
  39. 39.
    Macha IJ, Ozyegin LS, Chou J et al (2013) An alternative synthesis method for di calcium phosphate (monetite) powders from mediterranean mussel (mytilus galloprovincialis) shells. J Aust Ceram Soc 49:122–128Google Scholar
  40. 40.
    Aizenberg J, Hendler G (2004) Designing efficient microlens arrays: lessons from nature. J Mater Chem 14:2066–2072Google Scholar
  41. 41.
    White RA, Weber JN, White EW (1972) Replamineform: a new process for preparing porous ceramic, metal, and polymer prosthetic materials. Science 176:922–924Google Scholar
  42. 42.
    Raz S, Hamilton P, Wilt F et al (2003) The transient phase of amorphous calcium carbonate in sea urchin larval spicules: the involvement of proteins and magnesium ions in its formation and stabilization. Adv Funct Mater 13:480–486Google Scholar
  43. 43.
    Milev AS, Kannangara GSK, Ben-Nissan B (2003) Morphological stability of plate-like carbonated hydroxyapatite. Mater Lett 57:1960–1965Google Scholar
  44. 44.
    Samur R, Ozyegin L, Agaogullari D et al (2013) Calcium phosphate formation from sea urchin—(brissus latecarinatus) via modified mechano-chemical (ultrasonic) conversion method. Metalurgija 52:375–378Google Scholar
  45. 45.
    Demers C, Hamdy CR, Corsi K et al (2002) Natural coral exoskeleton as a bone graft substitute: a review. Biomed Mater Eng 12:15–35Google Scholar
  46. 46.
    Ben-Nissan B (2004) Nanoceramics in biomedical applications. MRS Bull 29:28–32Google Scholar
  47. 47.
    Ben-Nissan B, Choi AH (2006) Sol-gel production of bioactive nanocoatings for medical applications. Part 1: an introduction. Nanomedicine 1:311–319Google Scholar
  48. 48.
    Choi AH, Ben-Nissan B (2007) Sol-gel production of bioactive nanocoatings for medical applications. Part II: current research and development. Nanomedicine 2:51–61Google Scholar
  49. 49.
    Choi AH, Ben-Nissan B, Matinlinna JP et al (2013) Current perspectives: calcium phosphate nanocoatings and nanocomposite coatings in dentistry. J Dent Res 92:853–859Google Scholar
  50. 50.
    Choi AH, Ben-Nissan B (2015) Calcium phosphate nanocoatings and nanocomposites, part I: recent developments and advancements in tissue engineering and bioimaging. Nanomedicine 10:2249–2261Google Scholar
  51. 51.
    Ben-Nissan B, Macha I, Cazalbou S et al (2016) Calcium phosphate nanocoatings and nanocomposites, part 2: thin films for slow drug delivery and osteomyelitis. Nanomedicine 11:531–544Google Scholar
  52. 52.
    Birk RZ, Abramovitch-Gottlib L, Margalit I et al (2006) Conversion of adipogenic to osteogenic phenotype using crystalline porous biomatrices of marine origin. Tissue Eng 12:21–31Google Scholar
  53. 53.
    Ehrlich H, Etnoyer P, Litvinov SD et al (2006) Biomaterial structure in deep-sea bamboo coral (Anthozoa: Gorgonacea: Isididae): perspectives for the development of bone implants and templates for tissue engineering. Mat-wiss u Werkstofftech 37:552–557Google Scholar
  54. 54.
    Bonnelye E, Chabadel A, Saltel F et al (2008) Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42:129–138Google Scholar
  55. 55.
    Baudet-Pommel M, Collangettes-Peyrat D, Couvet-Lejczyk V (1988) Autotransplantation: clinical results, radiography, orthodontics, criteria for success. Actual Odontostomatol 163:463–472Google Scholar
  56. 56.
    Patat JL, Guillemin G (1989) Natural coral used as a replacement biomaterial in bone grafts. Ann Chir Plast Esthet 34:221–225Google Scholar
  57. 57.
    LeGeros RZ (1981) Apatites in biological systems. Prog Crystal Growth Charact 4:1–45Google Scholar
  58. 58.
    Papacharalambous SK, Anastasoff KI (1993) Natural coral skeleton used as onlay graft for contour augmentation of the face. A preliminary report. Int J Oral Maxillofac Surg 22:260–264Google Scholar
  59. 59.
    Ben-Nissan B, Milev A, Vago R (2004) Morphology of sol-gel derived nano-coated coralline hydroxyapatite. Biomaterials 25:4971–4975Google Scholar
  60. 60.
    Chou J, Ben-Nissan B, Choi AH et al (2007) Conversion of coral sand to calcium phosphate for biomedical application. J Aust Ceram Soc 43:44–48Google Scholar
  61. 61.
    Roy DM, Linnehan SK (1974) Hydroxyapatite formed from coral skeletal carbonate by hydrothermal exchange. Nature 247:220–222Google Scholar
  62. 62.
    Ben-Nissan B, Chai C, Evans L (1995) Crystallographic and spectroscopic characterisation and morphology of biogenic and synthetic apatites. In: Wise DL, Trantolo DJ, Altobelli MJ et al (eds) Encyclopedic handbook of biomaterials and bioengineering, vol 1B. Marcel Gekker Inc., New York, pp 191–221Google Scholar
  63. 63.
    Tang R, Hass M, Wu W et al (2003) Constant composition dissolution of mixed phases. II. Selective dissolution of calcium phosphates. J Colloid Interface Sci 260:379–384Google Scholar
  64. 64.
    Chou J, Hao J, Kuroda S et al (2013) Bone regeneration of rat tibial defect by zinc-tricalcium phosphate (Zn-TCP) synthesized from porous Foraminifera carbonate macrospheres. Mar Drugs 11:5148–5158Google Scholar
  65. 65.
    Chou J, Valenzuela SM, Santos J et al (2014) Strontium- and magnesium-enriched biomimetic β-TCP macrospheres with potential for bone tissue morphogenesis. J Tissue Eng Regen Med 8:771–778Google Scholar
  66. 66.
    Lopez E, Vidal B, Berland S et al (1992) Demonstration of the capacity of nacre to induce bone formation by human osteoblasts maintained in vitro. Tissue Cell 24:667–679Google Scholar
  67. 67.
    Lamghari M, Berland S, Laurent A et al (2001) Bone reactions to nacre injected percutaneously into the vertebrae of sheep. Biomaterials 22:555–562Google Scholar
  68. 68.
    Rousseau M, Pereira-Mouriès L, Almeida MJ et al (2003) The water-soluble matrix fraction from the nacre of Pinctada maxima produces earlier mineralization of MC3T3-E1 mouse pre-osteoblasts. Comp Biochem Physiol B: Biochem Mol Biol 135:1–7Google Scholar
  69. 69.
    Rousseau M, Boulzaguet H, Biagianti J et al (2008) Low molecular weight molecules of oyster nacre induce mineralization of the MC3T3-E1 cells. J Biomed Mater Res A 85(2):487–497Google Scholar
  70. 70.
    Duplat D, Chabadel A, Gallet M et al (2007) The in vitro osteoclastic degradation of nacre. Biomaterials 28:2155–2162Google Scholar
  71. 71.
    Westbroek P, Marin F (1988) A marriage of bone and nacre. Nature 392:861–862Google Scholar
  72. 72.
    Almeida MJ, Pereira L, Milet C et al (2001) Comparative effects of nacre water-soluble matrix and dexamethasone on the alkaline phosphatase activity of MRC-5 fibroblasts. J Biomed Mater Res 57:306–312Google Scholar
  73. 73.
    Zhang C, Li S, Ma Z et al (2006) A novel matrix protein p10 from the nacre of pearl oyster (Pinctada fucata) and its effects on both CaCO3 crystal formation and mineralogic cells. Marine Biotechnol 8:624–633Google Scholar
  74. 74.
    Liao H, Mutvei H, Hammarström L et al (2002) Tissue responses to nacreous implants in rat femur: an in situ hybridization and histochemical study. Biomaterials 23:2693–2701Google Scholar
  75. 75.
    Kim YW, Kim JJ, Kim YH et al (2002) Effects of organic matrix proteins on the interfacial structure at the bone-biocompatible nacre interface in vitro. Biomaterials 23:2089–2096Google Scholar
  76. 76.
    Chou J, Ben-Nissan B, Green DW et al (2011) Targeting and dissolution characteristics of bone forming and antibacterial drugs by harnessing the structure of microspherical shells from coral beach sand. Adv Eng Mater 13:93–99Google Scholar
  77. 77.
    Green DW, Li G, Milthorpe B et al (2012) Adult stem cell coatings for regenerative medicine. Mater Today 15:60–66Google Scholar
  78. 78.
    Chou J, Ito T, Bishop D et al (2013) Controlled release of simvastatin from biomimetic β-TCP drug delivery system. PLoS ONE 8:e54676.  https://doi.org/10.1371/journal.pone.0054676Google Scholar
  79. 79.
    Swatschek D, Schatton W, Kellermann J et al (2002) Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. Eur J Pharm Biopharm 53:107–113Google Scholar
  80. 80.
    Nicklas M, Schatton W, Heinemann S et al (2009) Preparation and characterization of marine sponge collagen nanoparticles and employment for the transdermal delivery of 17beta-estradiol-hemihydrate. Drug Dev Ind Pharm 35:1035–1042Google Scholar
  81. 81.
    Roberts P, Horner EA, Green DW et al (2008) Adipose tissue formation in vitro and in vivo using natural sea sponge and human bone marrow stromal cells. Eur Cell Mater 16:89Google Scholar
  82. 82.
    Boute N, Exposito JY, Boury-Esnault N et al (1996) Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol Cell 88:37–44Google Scholar

Copyright information

© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019

Authors and Affiliations

  • Besim Ben-Nissan
    • 1
    Email author
  • Andy H. Choi
    • 1
  • David W. Green
    • 1
  1. 1.School of Life Sciences, Biomaterials and Advanced Tissue EngineeringUniversity of Technology SydneySydneyAustralia

Personalised recommendations