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Algae-derived materials for tissue engineering and regenerative medicine applications: current trends and future perspectives

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Abstract

Algae are abundant and can be utilized as natural and cost-effective sources of potential biopolymers and biomaterials. Algae-derived polysaccharides with attractive similarity to the human extracellular matrix, unique chemical structures, efficient bioactive materials, significant biocompatibility/low toxicity, renewability, high biodegradability, colloidal characteristics, and moisture-retaining/swelling potentials can be employed as attractive materials for tissue engineering and regenerative medicine applications. Alginate, fucoidan, carrageenan, agarose, and ulvan with their unique physicochemical features and beneficial therapeutic activities have tissue engineering and regenerative medicine potentials. In this review, the main focus will be made on the important applications of algae for tissue engineering and regenerative medicine, and also important challenges and future perspectives are highlighted.

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References

  1. S. Iravani, R. Varma, Plant-derived edible nanoparticles and miRNAs: emerging frontier for therapeutics and targeted drug-delivery. ACS Sustain. Chem. Eng. 7, 8055–8069 (2019)

    Article  CAS  Google Scholar 

  2. S. Iravani, R.S. Varma, Plants and plant-based polymers as scaffolds for tissue engineering. Green Chem. 21, 4839–4867 (2019)

    Article  CAS  Google Scholar 

  3. S. Iravani, R.S. Varma, Greener synthesis of lignin nanoparticles and their applications. Green Chem. 22, 612–636 (2020)

    Article  CAS  Google Scholar 

  4. S. Iravani, R.S. Varma, MXenes and MXene-based materials for tissue engineering and regenerative medicine: recent advances. Mater. Adv. 2, 2906–2917 (2021)

    Article  CAS  Google Scholar 

  5. J.M. Dang, K.W. Leong, Natural polymers for gene delivery and tissue engineering. Adv. Drug Deliv. Rev. 58, 487–499 (2006)

    Article  CAS  Google Scholar 

  6. K.Y. Lee, D.J. Mooney, Hydrogels for tissue engineering. Chem. Rev. 101, 1869–1879 (2001)

    Article  CAS  Google Scholar 

  7. D.A. Taylor, L.C. Sampaio, Z. Ferdous, A.S. Gobin, L.J. Taite, Decellularized matrices in regenerative medicine. Acta Biomater. 74, 74–89 (2018)

    Article  CAS  Google Scholar 

  8. J.P. Vacanti, R. Langer, Tissue engineering: the design and fabrication of living replacement devices for surgical reconstruction and transplantation. Lancet 354, SI32–SI34 (1999)

    Article  Google Scholar 

  9. A.J. Salgado, O.P. Coutinho, R.L. Reis, Bone tissue engineering: state of the art and future trends. Macromol Biosci 4, 743–65 (2004)

  10. S. Pina, V.P. Ribeiro, C.F. Marques, F.R. Maia, T.H. Silva, R.L. Reis, J.M. Oliveira, Scaffolding strategies for tissue engineering and regenerative medicine applications. Materials 12, 1824 (2019). https://doi.org/10.3390/ma12111824

    Article  CAS  Google Scholar 

  11. A. van der Smissen, V. Hintze, D. Scharnweber, S. Moeller, M. Schnabelrauch, A. Majok, J.C. Simon, U. Anderegg, Growth promoting substrates for human dermal fibroblasts provided by artificial extracellular matrices composed of collagen I and sulfated glycosaminoglycans. Biomaterials 32, 8938–8946 (2011)

    Article  CAS  Google Scholar 

  12. J. Salbach, T.D. Rachner, M. Rauner, U. Hempel, U. Anderegg, S. Franz, J.C. Simon, L.C. Hofbauer, Regenerative potential of glycosaminoglycans for skin and bone. J. Mol. Med. (Berl) 90, 625–635 (2012)

    Article  Google Scholar 

  13. L. Ma, C. Gao, Z. Mao, J. Zhou, J. Shen, X. Hu, C. Han, Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 24, 4833–4841 (2003)

    Article  CAS  Google Scholar 

  14. K. Senni, J. Pereira, F. Gueniche, C. Delbarre-Ladrat, C. Sinquin, J. Ratiskol, G. Godeau, A.-M. Fischer, D. Helley, S. Colliec-Jouault, Marine polysaccharides: a source of bioactive molecules for cell therapy and tissue engineering. Mar. Drugs 9, 1664–1681 (2011)

    Article  CAS  Google Scholar 

  15. T.H. Silva, A. Alves, B.M. Ferreira, J.M. Oliveira, L.L. Reys, R.F. Ferreira, R.A. Souza, S.S. Silva, J.F. Mano, R.L. Reis, Materials of marine origin: a review on polymers and ceramics of biomedical interest. Mater. Rev. 57, 276–306 (2012)

    Article  CAS  Google Scholar 

  16. M. Shanmugam, B.K. Ramavat, K.H. Mody, R.M. Oza, A. Tewari, Distribution of heparinoid-active sulphated polysaccharides in some Indian marine green algae. Indian J. Mar. Sci.30, 222–227 (2001)

    Google Scholar 

  17. G. Toskas, R.-D. Hund, E. Laourine, C. Cherif, V. Smyrniotopoulos, V. Roussis, Nanobers based on polysaccharides from the green seaweed Ulva Rigida. Carbohydr. Polym. 84, 1093–1102 (2011)

    Article  CAS  Google Scholar 

  18. L. Yang, L.-M. Zhang, Chemical structural and chain conformational characterization of some bioactive polysaccharides isolated from natural sources. Carbohydr. Polym. 76, 349–361 (2009)

    Article  CAS  Google Scholar 

  19. I.S. Fernando, K.A. Sanjeewa, K.W. Samarakoon, W.W. Lee, H.S. Kim, E.A. Kim, U.K. Gunasekara, D.T. Abeytunga, C. Nanayakkara, E.D. de Silva, H.S. Lee, FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae 32, 75–86 (2017)

    Article  CAS  Google Scholar 

  20. O.S. Vishchuk, D.V. Tarbeeva, S.P. Ermakova, T.N. Zvyagintseva, Structural characteristics and biological activity of fucoidans from the brown algae Alaria sp. and Saccharina japonica of different reproductive status. Chem. Biodiversity 9, 817–828 (2012)

    Article  CAS  Google Scholar 

  21. N.E. Ustyuzhanina, M.I. Bilan, A.G. Gerbst, N.A. Ushakova, E.A. Tsvetkova, A.S. Dmitrenok, A.I. Usov, N.E. Nifantiev, Anticoagulant and antithrombotic activities of modified xylofucan sulfate from the brown alga Punctaria plantaginea. Carbohyd. Polym. 136, 826–833 (2016)

    Article  CAS  Google Scholar 

  22. S. Koyanagi, N. Tanigawa, H. Nakagawa, S. Soeda, H. Shimeno, Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem. Pharmacol. 65, 173–179 (2003)

    Article  CAS  Google Scholar 

  23. N.J. Borazjani, M. Tabarsa, S. You, M. Rezaei, Improved immunomodulatory and antioxidant properties of unrefined fucoidans from Sargassum angustifolium by hydrolysis. J. Food Sci. Technol. 54, 4016–4025 (2017)

    Article  CAS  Google Scholar 

  24. A.C. Hernández-González, L. Téllez-Jurado, L.M. Rodríguez-Lorenzo, Alginate hydrogels for bone tissue engineering, from injectables to bioprinting: a review. Carbohydr. Polym. 229, 115514 (2020)

    Article  CAS  Google Scholar 

  25. A.D. Sezer, F. Hatipoglu, E. Cevher, Z. Oğurtan, A.L. Baş, J. Akbuğa, Chitosan film containing fucoidan as a wound dressing for dermal burn healing: preparation and in vitro/in vivo evaluation. AAPS PharmSciTech 8, E94-101 (2007)

    Article  Google Scholar 

  26. K. Murakami, H. Aoki, S. Nakamura, S. Nakamura, M. Takikawa, M. Hanzawa, S. Kishimoto, H. Hattori, Y. Tanaka, T. Kiyosawa, Y. Sato, M. Ishihara, Hydrogel blends of chitin/chitosan, fucoidan and alginate as healingimpaired wound dressings. Biomaterials 31, 83–90 (2010)

    Article  CAS  Google Scholar 

  27. G. Jin, G.H. Kim, Rapid-prototyped PCL/fucoidan composite scaffolds for bone tissue regeneration: design, fabrication, and physical/biological properties. J. Mater. Chem. 21, 17710–17718 (2011)

    Article  CAS  Google Scholar 

  28. J.S. Lee, G.H. Jin, M.G. Yeo, C.H. Jang, H. Lee, G.H. Kim, Fabrication of electrospun biocomposites comprising polycaprolactone/fucoidan for tissue regeneration. Carbohydr. Polym. 90, 181–188 (2012)

    Article  CAS  Google Scholar 

  29. A.D. Sezer, E. Cevher, F. Hatipoğlu, Z. Oğurtan, A.L. Baş, J. Akbuğa, Preparation of fucoidan-chitosan hydrogel and its application as burn healing accelerator on rabbits. Biol. Pharm. Bull. 31, 2326–2333 (2008)

    Article  CAS  Google Scholar 

  30. S.I.T. Changotade, G. Korb, J. Bassil, B. Barroukh, C. Willig, S. Colliec-Jouault, P. Durand, G. Godeau, K. Senni, Potential effects of a low-molecular-weight fucoidan extracted from brown algae on bone biomaterial osteoconductive properties. J. Biomed. Mater. Res. A 87A, 666–675 (2008)

    Article  CAS  Google Scholar 

  31. F.L. Wang, H. Schmidt, D. Pavleska, T. Wermann, A. Seekamp, S. Fuchs, Crude fucoidan extracts impair angiogenesis in models relevant for bone regeneration and osteosarcoma via reduction of VEGF and SDF-1. Mar. Drugs 15, 186 (2017)

    Article  CAS  Google Scholar 

  32. J. Pereira, S. Portron, B. Dizier, C. Vinatier, M. Masson, S. Sourice, I. Galy-Fauroux, P. Corre, P. Weiss, A.M. Fischer, J. Guicheux, D. Helley, The in vitro and in vivo effects of a low-molecularweight fucoidan on the osteogenic capacity of human adipose-derived stromal cells. Tissue Eng. Pt. A 20, 275–284 (2014)

    Article  CAS  Google Scholar 

  33. J. Venkatesan, I. Bhatnagar, S.-K. Kim, Chitosan-alginate biocomposite containing fucoidan for bone tissue engineering Mar. Drugs 12, 300–316 (2014)

    CAS  Google Scholar 

  34. H.S. Jeong, J. Venkatesan, S.K. Kim, Hydroxyapatite-fucoidan nanocomposites for bone tissue engineering. Int. J. Biol. Macromol. 57, 138–141 (2013)

    Article  CAS  Google Scholar 

  35. S. Puvaneswary, S. Talebian, H.B. Raghavendran, M.R. Murali, M. Mehrali, A.M. Afifi, N.H.B. Abu Kasim, T. Kamarul, Fabrication and in vitro biological activity of beta TCP-chitosan-fucoidan composite for bone tissue engineering. Carbohydr. Polym. 134, 799–807 (2015)

    Article  CAS  Google Scholar 

  36. T.Y. Ahn, J.H. Kang, D.J. Kang, J. Venkatesan, H.K. Chang, I. Bhatnagar, K.Y. Chang, J.H. Hwang, Z. Salameh, S.K. Kim, H.T. Kim, D.G. Kim, Interaction of stem cells with nano hydroxyapatite-fucoidan bionanocomposites for bone tissue regeneration. Int. J. Biol. Macromol. 93, 1488–1491 (2016)

    Article  CAS  Google Scholar 

  37. S. Puvaneswary, H.B. Raghavendran, S. Talebian, M.R. Murali, S.A. Mahmod, S. Singh, T. Kamarul, Incorporation of fucoidan in beta-tricalcium phosphate-chitosan scaffold prompts the differentiation of human bone marrow stromal cells into osteogenic lineage. Sci. Rep. 6, 1–111 (2016)

  38. H.-T. Lu, T.-W. Lu, C.-H. Chen, K.-Y. Lu, F.-L. Mi, Development of nanocomposite scaffolds based on biomineralization of N, O-carboxymethyl chitosan/fucoidan conjugates for bone tissue engineering. Int. J. Biol. Macromol. 120, 2335–2345 (2018)

    Article  CAS  Google Scholar 

  39. B. Lowe, J. Venkatesan, S. Anil, M.S. Shim, S.-K. Kim, Preparation and characterization of chitosan-natural nano hydroxyapatite-fucoidan nanocomposites for bone tissue engineering. Int. J. Biol. Macromol. 93, 1479–1487 (2016)

    Article  CAS  Google Scholar 

  40. W. Zhang, L. Zhao, J. Ma, X. Wang, Y. Wang, F. Ran, Y. Wang, H. Ma, S. Yu, Electrospinning of fucoidan/chitosan/poly(vinyl alcohol) scaffolds for vascular tissue engineering. Fibers Polymers 18, 922–932 (2017)

    Article  CAS  Google Scholar 

  41. D.N. Carvalho, R. López-Cebral, R.O. Sousa, A.L. Alves, L.L. Reys, S.S. Silva, J.M. Oliveira, R.L. Reis, T.H. Silva, Marine collagen-chitosan-fucoidan cryogels as cell-laden biocomposites envisaging tissue engineering. Biomed. Mater. 15, 055030 (2020)

    Article  CAS  Google Scholar 

  42. M.L. Amin, D. Mawad, S. Dokos, P. Koshy, P.J. Martens, C.C. Sorrell, Immunomodulatory properties of photopolymerizable fucoidan and carrageenans. 230, 115691 (2020)

  43. S.M. Mihaila, A.K. Gaharwar, R.L. Reis, A.P. Marques, M.E. Gomes, A. Khademhosseini, Photocrosslinkable kappa-carrageenan hydrogels for tissue engineering applications. Adv. Healthc. Mater. 2, 895–907 (2013)

    Article  CAS  Google Scholar 

  44. L. Tytgat, M. Vagenende, H. Declercq, J.C. Martins, H. Thienpont, H. Ottevaere, P. Dubruel, S. Van Vlierberghe, Synergistic effect of κ-carrageenan and gelatin blends towards adipose tissue engineering. Carbohyd. Polym. 189, 1–9 (2018)

    Article  CAS  Google Scholar 

  45. P. Jiang, C. Yan, Y. Guo, X. Zhang, M. Cai, X. Jia, X. Wang, F. Zhoua, Direct ink writing with high-strength and swelling-resistant biocompatible physically crosslinked hydrogels. Biomater. Sci. 7, 1805–1814 (2019)

    Article  CAS  Google Scholar 

  46. S.A. Wilson, L.M. Cross, C.W. Peak, A.K. Gaharwar, Shear-Thinning and thermo-reversible nanoengineered inks for 3D bioprinting. ACS Appl. Mater. Interfaces 9, 43449–43458 (2017)

    Article  CAS  Google Scholar 

  47. H. Li, Y.J. Tan, L. Li, A strategy for strong interface bonding by 3D bioprinting of oppositely charged κ-carrageenan and gelatin hydrogels. Carbohydr. Polym. 198, 261–269 (2018)

    Article  CAS  Google Scholar 

  48. L. Tytgat, L. Van Damme, M.D.P. Ortega Arevalo, H. Declercq, H. Thienpont, H. Otteveare, P. Blondeel, P. Dubruel, S. Van Vlierberghe, Extrusion-based 3D printing of photo-crosslinkable gelatin and κ-carrageenan hydrogel blends for adipose tissue regeneration. Int. J. Biol. Macromol. 140, 929–938 (2019)

    Article  CAS  Google Scholar 

  49. P.M. Rocha, V.E. Santo, M.E. Gomes, R.L. Reis, J.F. Mano, Encapsulation of adipose-derived stem cells and transforming growth factor-β1 in carrageenan-based hydrogels for cartilage tissue engineering. J. Bioact. Compat. Polym. 26, 493–507 (2011)

    Article  CAS  Google Scholar 

  50. V.E. Santo, A.M. Frias, M. Carida, R. Cancedda, M.E. Gomes, J.F. Mano, R.L. Reis, Carrageenan-based hydrogels for the controlled delivery of PDGF-BB in bone tissue engineering applications. Biomacromol 10, 1392–1401 (2009)

    Article  CAS  Google Scholar 

  51. G.T. İlhan, G. Irmak, M. Gümüşderelioğlu, Microwave assisted methacrylation of Kappa carrageenan: a bioink for cartilage tissue engineering. Int. J. Biol. Macromol. 164, 3523–3534 (2020)

    Article  CAS  Google Scholar 

  52. X. Qi, T. Su, M. Zhang, X. Tong, W. Pan, Q. Zeng, Z. Zhou, L. Shen, X. He, J. Shen, Macroporous hydrogel scaffolds with tunable physicochemical properties for tissue engineering constructed using renewable polysaccharides. ACS Appl. Mater. Interfaces 12, 13256–13264 (2020)

    Article  CAS  Google Scholar 

  53. S. Mirza, R. Jolly, I. Zia, M.S. Umar, M. Owais, M. Shakir, Bioactive gum Arabic/κ-carrageenan-incorporated nano-hydroxyapatite nanocomposites and their relative biological functionalities in bone tissue engineering. ACS Omega 5, 11279–11290 (2020)

    Article  CAS  Google Scholar 

  54. R. Yegappan, V. Selvaprithiviraj, S. Amirthalingam, A. Mohandas, N.S. Hwang, R. Jayakumar, Injectable angiogenic and osteogenic carrageenan nanocomposite hydrogel for bone tissue engineering. Int. J. Biol. Macromol. 122, 320–328 (2019)

    Article  CAS  Google Scholar 

  55. N. Pettinelli, S. Rodríguez-Llamazares, R. Bouza, L. Barral, S. Feijoo-Bandín, F. Lago, Carrageenan-based physically crosslinked injectable hydrogel for wound healing and tissue repairing applications. Int. J. Pharm. 589, 119828 (2020)

    Article  CAS  Google Scholar 

  56. T.G. Polat, O. Duman, S. Tunç, Agar/κ-carrageenan/montmorillonite nanocomposite hydrogels for wound dressing applications. Int. J. Biol. Macromol. 164, 4591–4602 (2020)

    Article  CAS  Google Scholar 

  57. T.G. Polat, O. Duman, S. Tunç, Preparation and characterization of environmentally friendly agar/κ-carrageenan/montmorillonite nanocomposite hydrogels. Colloids Surf. A Physicochem. Eng. Asp. 602, 124987 (2020)

  58. E.G. Popa, S.G. Caridade, J.F. Mano, R.L. Reis, M.E. Gomes, Chondrogenic potential of injectable κ-carrageenan hydrogel with encapsulated adipose stem cells for cartilage tissue-engineering applications. J. Tissue Eng. Regen. Med. 9, 550–563 (2015)

    Article  CAS  Google Scholar 

  59. L. Tytgat, L.V. Damme, M.P.O. Arevalo, H. Declercq, H. Thienpont, H. Otteveare, P. Blondeel, P. Dubruel, S.V. Vlierberghe, Extrusion-based 3D printing of photo-crosslinkable gelatin and κ-carrageenan hydrogel blends for adipose tissue regeneration. Int. J. Biol. Macromol. 140, 929–938 (2019)

    Article  CAS  Google Scholar 

  60. S. Tavakoli, M. Kharaziha, A. Kermanpur, H. Mokhtari, Sprayable and injectable visible-light Kappa-carrageenan hydrogel for in-situ soft tissue engineering. Int. J. Biol. Macromol. 138, 590–601 (2019)

    Article  CAS  Google Scholar 

  61. K.Y. Lee, D.J. Mooney, Alginate: properties and biomedical applications. Prog. Polym. Sci. 37, 106–126 (2012)

    Article  CAS  Google Scholar 

  62. M.A. Taemeh, A. Shiravandi, M. Asadi Korayem, H. Daemi, Fabrication challenges and trends in biomedical applications of alginate electrospun nanofibers. Carbohyd. Polym. 228, 115419 (2020)

    Article  CAS  Google Scholar 

  63. S. Datta, A. Das, P. Sasmal, S. Bhutoria, A.R. Chowdhury, P. Datta, Alginate-poly(amino acid) extrusion printed scaffolds for tissue engineering applications. Int. J. Polym. Mater. Polym. Biomater. 69, 65–72 (2020)

    Article  CAS  Google Scholar 

  64. N. Raja, H.S. Yun, A simultaneous 3D printing process for the fabrication of bioceramic and cell-laden hydrogel core/shell scaffolds with potential application in bone tissue regeneration. J. Mater. Chem. B 4, 4707–4716 (2016)

    Article  CAS  Google Scholar 

  65. Y.B. Kim, H. Lee, G.H. Yang, C.H. Choi, D. Lee, H. Hwang, W.K. Jung, H. Yoon, G.H. Kim, Mechanically reinforced cell-laden scaffolds formed using alginate-based bioink printed onto the surface of a PCL/alginate mesh structure for regeneration of hard tissue. J. Colloid Interface Sci. 461, 359–368 (2016)

    Article  CAS  Google Scholar 

  66. L. Ouyang, R. Yao, Y. Zhao, W. Sun, Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells. Biofabrication 8, 035020 (2016)

    Article  CAS  Google Scholar 

  67. J. Park, S.J. Lee, S. Chung, J.H. Lee, W.D. Kim, J.Y. Lee, S.A. Park, Cell-laden 3D bioprinting hydrogel matrix depending on different compositions for soft tissue engineering. Mater. Sci. Eng. C Mater. Biol. Appl. 71, 678–684 (2017)

    Article  CAS  Google Scholar 

  68. Q. Gu, E. Tomaskovic-Crook, G.G. Wallace, J.M. Crook, 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv. Healthc. Mater. 6, 1700175 (2017)

    Article  CAS  Google Scholar 

  69. Z. Li, S. Huang, Y. Liu, B. Yao, T. Hu, H. Shi, J. Xie, X. Fu, Tuning alginate-gelatin bioink properties by varying solvent and their impact on stem cell behavior. Sci. Rep. 8, 8020 (2018)

    Article  CAS  Google Scholar 

  70. Q. Gu, E. Tomaskovic-Crook, R. Lozano, Y. Chen, R.M. Kapsa, Q. Zhou, G.G. Wallace, J.M. Crook, Functional 3D neural mini-tissues from printed gel-based bioink and human neural stem cells. Adv. Healthc. Mater. 5, 1429–1438 (2016)

    Article  CAS  Google Scholar 

  71. E. Hodder, S. Duin, D. Kilian, T. Ahlfeld, J. Seidel, C. Nachtigall, P. Bush, D. Covill, M. Gelinsky, A. Lode, Investigating the effect of sterilisation methods on the physical properties and cytocompatibility of methyl cellulose used in combination with alginate for 3D-bioplotting of chondrocytes. J. Mater. Sci. Mater. Med. 30 (2019). https://doi.org/10.1007/s10856-10018-16211-10859

  72. B. Yao, T. Hu, X. Cui, W. Song, X. Fu, S. Huang, Enzymatically degradable alginate/gelatin bioink promotes cellular behavior and degradation in vitro and in vivo. Biofabrication 11, 045020 (2019)

    Article  CAS  Google Scholar 

  73. G. Choe, S. Oh, J.M. Seok, S.A. Park, J.Y. Lee, Graphene oxide/alginate composites as novel bioinks for three-dimensional mesenchymal stem cell printing and bone regeneration applications. Nanoscale 11, 23275–23285 (2019)

    Article  CAS  Google Scholar 

  74. J. Zhang, E. Wehrle, J.R. Vetsch, G.R. Paul, M. Rubert, R. Müller, Alginate dependent changes of physical properties in 3D bioprinted cell-laden porous scaffolds affect cell viability and cell morphology. Biomed. Mater. 14, 065009 (2019)

    Article  CAS  Google Scholar 

  75. V. Fantini, M. Bordoni, F. Scocozza, M. Conti, E. Scarian, S. Carelli, A.M. Di Giulio, S. Marconi, O. Pansarasa, F. Auricchio, C. Cereda, Bioink composition and printing parameters for 3D modeling neural tissue. Cells 8, 830 (2019)

    Article  CAS  Google Scholar 

  76. M.H. Kim, Y.W. Lee, W.K. Jung, J. Oh, S.Y. Nam, Enhanced rheological behaviors of alginate hydrogels with carrageenan for extrusion-based bioprinting. J. Mech. Behav. Biomed. Mater. 98, 187–194 (2019)

    Article  CAS  Google Scholar 

  77. J.M. Baena, G. Jiménez, E. López-Ruiz, C. Antich, C. Griñán-Lisón, M. Perán, P. Gálvez-Martín, J.A. Marchal, Volume-by-volume bioprinting of chondrocytes-alginate bioinks in high temperature thermoplastic scaffolds for cartilage regeneration. Exp. Biol. Med. (Maywood) 244, 13–21 (2019)

    Article  CAS  Google Scholar 

  78. L. Li, S. Qin, J. Peng, A. Chen, Y. Nie, T. Liu, K. Song, Engineering gelatin-based alginate/carbon nanotubes blend bioink for direct 3D printing of vessel constructs. Int. J. Biol. Macromol. 145, 262–271 (2020)

    Article  CAS  Google Scholar 

  79. C. Henrionnet, L. Pourchet, P. Neybecker, O. Messaoudi, P. Gillet, D. Loeuille, D. Mainard, C. Marquette, A. Pinzano, Combining innovative bioink and low cell density for the production of 3d-bioprinted cartilage substitutes: a pilot study. Stem Cells Int. 2020, 2487072 (2020)

    Article  CAS  Google Scholar 

  80. C.J. Wright, B.Z. Molino, J.H.Y. Chung, J.T. Pannell, M. Kuester, P.J. Molino, T.W. Hanks, Synthesis and 3D printing of conducting alginate-polypyrrole ionomers. Gels 6, E13 (2020)

    Article  CAS  Google Scholar 

  81. D. Kilian, T. Ahlfeld, A.R. Akkineni, A. Bernhardt, M. Gelinsky, A. Lode, 3D bioprinting of osteochondral tissue substitutes - in vitro-chondrogenesis in multi-layered mineralized constructs. Sci. Rep. 10, 8277 (2020)

    Article  CAS  Google Scholar 

  82. Z. Li, H.R. Ramay, K.D. Hauch, D. Xiao, M. Zhang, Chitosan–alginate hybrid scaffolds for bone tissue engineering. Biomaterials 26, 3919–3928 (2005)

    Article  CAS  Google Scholar 

  83. J. Venkatesan, I. Bhatnagar, P. Manivasagan, K.-H. Kang, S.-K. Kim, Alginate composites for bone tissue engineering: a review. Int. J. Biol. Macromol. 72, 269–281 (2015)

    Article  CAS  Google Scholar 

  84. B.K. Shanmugam, S. Rangaraj, K. Subramani, S. Srinivasan, W.K. Aicher, R. Venkatachalam, Biomimetic TiO2-chitosan/sodium alginate blended nanocomposite scaffolds for tissue engineering applications. Mater. Sci. Eng. C 110, 110710 (2020)

    Article  CAS  Google Scholar 

  85. S.D. Purohit, R. Bhaskar, H. Singh, I. Yadav, M.K. Gupta, N.C. Mishra, Development of a nanocomposite scaffold of gelatin–alginate–graphene oxide for bone tissue engineering. Int. J. Biol. Macromol. 133, 592–602 (2019)

    Article  CAS  Google Scholar 

  86. J. Li, X. Liu, J.M. Crook, G.G. Wallace, 3D printing of cytocompatible graphene/alginate scaffolds for mimetic tissue constructs. Front. Bioeng. Biotechnol. (2020). https://doi.org/10.3389/fbioe.2020.00824

    Article  Google Scholar 

  87. M.M. Pérez-Madrigal, J.E. Shaw, M.C. Arno, J.A. Hoyland, S.M. Richardson, A.P. Dove, Robust alginate/hyaluronic acid thiol–yne click-hydrogel scaffolds with superior mechanical performance and stability for load-bearing soft tissue engineering†. Biomater. Sci. 8, 405–412 (2020)

    Article  Google Scholar 

  88. M. Hajiabbas, I. Alemzadeh, M. Vossoughi, A porous hydrogel-electrospun composite scaffold made of oxidized alginate/gelatin/silk fibroin for tissue engineering application. Carbohydr. Polym. 245, 116465 (2020)

    Article  CAS  Google Scholar 

  89. T. Chae, H. Yang, H. Moon, T. Troczynski, F.K. Ko, Biomimetically mineralized alginate nanocomposite fibers for bone tissue engineering: mechanical properties and in vitro cellular interactions. ACS Appl. Bio. Mater. (2020). https://doi.org/10.1021/acsabm.0c00692

    Article  Google Scholar 

  90. S. Irani, S. Tavakkoli, M. Pezeshki‐Modaress, E. Taghavifar, M. Mohammadali, H. Daemi, Electrospun nanofibrous alginate sulfate scaffolds promote mesenchymal stem cells differentiation to chondrocytes. J. Appl. Polym. Sci. 138, 1–12 (2021). https://doi.org/10.1002/app.49868

  91. D. Suárez-González, K. Barnhart, E. Saito, R. Vanderby Jr., S.J. Hollister, W.L. Murphy, Controlled nucleation of hydroxyapatite on alginate scaffolds for stem cell-based bone tissue engineering. J. Biomed. Mater. Res. Part A 95A, 222–234 (2010)

    Article  CAS  Google Scholar 

  92. T. Pan, W. Song, X. Cao, Y. Wang, 3D bioplotting of gelatin/alginate scaffolds for tissue engineering: influence of crosslinking degree and pore architecture on physicochemical properties. J. Mater. Sci. Technol. 32, 889–900 (2016)

    Article  CAS  Google Scholar 

  93. P.N. Sudha, T. Gomathi, S.K. Kim, Ulvan in tissue engineering, in: S.K. Kim (Ed.) Encyclopedia of Marine Biotechnology, 1335-1350 (John Wiley & Sons Ltd, 2020)

  94. M. Dash, S.K. Samal, C. Bartoli, A. Morelli, P.F. Smet, P. Dubruel, F. Chiellini, Biofunctionalization of ulvan scaffolds for bone tissue engineering. ACS Appl. Mater. Interfaces 6, 3211–3218 (2014)

    Article  CAS  Google Scholar 

  95. T.K. Gajaria, H. Bhatt, A. Khandelwal, V.T. Vasu, C.R.K. Reddy, D.S. Lakshmi, A facile chemical cross-linking approach toward the fabrication of a sustainable porous ulvan scaffold. J. Bioact. Compat. Polym. (2020). https://doi.org/10.1177/0883911520939986

    Article  Google Scholar 

  96. H.C. Moon, H. Choi, S. Kikionis, J. Seo, W. Youn, E. Ioannou, S.Y. Han, H. Cho, V. Roussis, I.S. Choi, Fabrication and characterization of neurocompatible ulvan-based layer-by-layer films. Langmuir (2020). https://doi.org/10.1021/acs.langmuir.0c02173

    Article  Google Scholar 

  97. A. Alves, A.R.C. Duarte, J.F. Mano, R.A. Sousa, R.L. Reis, PDLLA enriched with ulvan particles as a novel 3D porous scaffold targeted for bone engineering. J. Supercrit. Fluids 65, 32–38 (2012)

    Article  CAS  Google Scholar 

  98. A. Alves, R.A. Sousa, R.L. Reis, Processing of degradable ulvan 3D porous structures for biomedical applications. J. Biomed. Mater. Res. Part. A 101A, 998–1006 (2013)

    Article  CAS  Google Scholar 

  99. L.-A. Tziveleka, A. Sapalidis, S. Kikionis, E. Aggelidou, E. Demiri, A. Kritis, E. Ioannou, V. Roussis, Hybrid sponge-like scaffolds based on ulvan and gelatin: design, characterization and evaluation of their potential use in bone tissue. Eng. Mater. 13, 1763 (2020)

    CAS  Google Scholar 

  100. G. Toskas, S. Heinemann, C. Heinemann, C. Cherif, R.-D. Hund, V. Roussis, T. Hanke, Ulvan and ulvan/chitosan polyelectrolyte nanofibrous membranes as a potential substrate material for the cultivation of osteoblasts. Carbohyd. Polym. 89, 997–1002 (2012)

    Article  CAS  Google Scholar 

  101. A. Alves, E.D. Pinho, N.M. Neves, R.A. Sousa, R.L. Reis, Processing ulvan into 2D structures: cross-linked ulvan membranes as new biomaterials for drug delivery applications. Int. J. Pharm. 426, 76–81 (2012)

    Article  CAS  Google Scholar 

  102. A. Alves, R.A. Sousa, R.L. Reis, Processing of degradable ulvan 3D porous structures for biomedical applications. J. Biomed. Mater. Res. A 101, 998–1006 (2013)

    Article  CAS  Google Scholar 

  103. J. Gopinathan, I. Noh, Recent trends in bioinks for 3D printing. Biomater. Res. 22, 11 (2018). https://doi.org/10.1186/s40824-40018-40122-40821

    Article  Google Scholar 

  104. P. Zarrintaj, S. Manouchehri, Z. Ahmadi, M.R. Saeb, A.M. Urbanska, D.L. Kaplan, M. Mozafari, Agarose-based biomaterials for tissue engineering. Carbohyd. Polym. 187, 66–84 (2018)

    Article  CAS  Google Scholar 

  105. D.Y. Lewitus, J. Landers, J.R. Branch, K.L. Smith, G. Callegari, J. Kohn, A.V. Neimark, Biohybrid carbon nanotube/agarose fibers for neural tissue engineering. Adv. Funct. Mater. 21, 2624–2632 (2011)

    Article  CAS  Google Scholar 

  106. F. Yang, Y. Zhang, B. Liu, M. Cao, J. Yang, F. Tian, P. Yang, K. Qin, D. Zhao, Basic fibroblast growth factor and agarose gel promote the ability of immune privilege of allogeneic cartilage transplantation in rats. J. Orthopaedic Transl. 22, 73–80 (2020)

    Article  Google Scholar 

  107. D.F. Duarte Campos, A. Blaeser, M. Weber, J. Jäkel, S. Neuss, W. Jahnen-Dechent, H. Fischer, Three-dimensional printing of stem cell-laden hydrogels submerged in a hydrophobic high-density fluid. Biofabrication 5, 015003 (2013)

    Article  CAS  Google Scholar 

  108. D.F. Duarte Campos, A. Blaeser, A. Korsten, S. Neuss, J. Jäkel, M. Vogt, H. Fischer, The stiffness and structure of three-dimensional printed hydrogels direct the differentiation of mesenchymal stromal cells toward adipogenic and osteogenic lineages. Tissue Eng. Part A 21, 740–756 (2015)

    Article  CAS  Google Scholar 

  109. R. Fan, M. Piou, E. Darling, D. Cormier, J. Sun, J. Wan, Bio-printing cell-laden matrigel-agarose constructs. J. Biomater. Appl. 31, 684–692 (2016)

    Article  CAS  Google Scholar 

  110. M. Köpf, D.F. Duarte Campos, A. Blaeser, K.S. Sen, H. Fischer, A tailored three-dimensionally printable agarose-collagen blend allows encapsulation, spreading, and attachment of human umbilical artery smooth muscle cells. Biofabrication 8, 025011 (2016)

    Article  CAS  Google Scholar 

  111. D.F. Duarte Campos, A. Blaeser, K. Buellesbach, K.S. Sen, W. Xun, W. Tillmann, H. Fischer, Bioprinting organotypic hydrogels with improved mesenchymal stem cell remodeling and mineralization properties for bone tissue. Eng. Adv. Healthc. Mater. 5, 1336–1345 (2016)

    Article  CAS  Google Scholar 

  112. A. Forget, A. Blaeser, F. Miessmer, M. Köpf, D.F. Duarte Campos, N.H. Voelcker, A. Blencowe, H. Fischer, V. Shastri, Mechanically tunable bioink for 3D bioprinting of human cells. Adv. Healthc. Mater. 6, 1700255 (2017)

    Article  CAS  Google Scholar 

  113. F. Kreimendahl, M. Köpf, A.L. Thiebes, D.F. Duarte Campos, A. Blaeser, T. Schmitz-Rode, C. Apel, S. Jockenhoevel, H. Fischer, Three-dimensional printing and angiogenesis: tailored agarose-type I collagen blends comprise three-dimensional printability and angiogenesis potential for tissue-engineered substitutes tissue. Eng. Part C Methods 23, 604–615 (2017)

    Article  CAS  Google Scholar 

  114. Z. Atoufi, P. Zarrintaj, G.H. Motlagh, A. Amiri, Z. Bagher, S.K. Kamrava, A novel bio electro active alginate-aniline tetramer/ agarose scaffold for tissue engineering: synthesis, characterization, drug release and cell culture study. J. Biomater. Sci. Polym. Ed. 28, 1617–1638 (2017)

    Article  CAS  Google Scholar 

  115. B. Bagheri, P. Zarrintaj, S.S. Surwase, N. Baheiraei, M.R. Saeb, M. Mozafari, Y.C. Kim, O.O. Park, Self-gelling electroactive hydrogels based on chitosan–aniline oligomers/agarose for neural tissue engineering with on-demand drug release. Colloids Surfaces B: Biointerfaces 184, 110549 (2019)

    Article  CAS  Google Scholar 

  116. S.S. Garakani, M. Khanmohammadi, Z. Atoufi, S.K. Kamrava, M. Setayeshmehr, R. Alizadeh, F. Faghihi, Z. Bagher, S.M. Davachi, A. Abbaspourrad, Fabrication of chitosan/agarose scaffolds containing extracellular matrix for tissue engineering applications. Int. J. Biol. Macromol. 143, 533–545 (2020)

    Article  CAS  Google Scholar 

  117. A.B. Bonhome-Espinosa, F. Campos, D. Durand-Herrera, J.D. Sánchez-López, S. Schaub, J.D.G. Durán, M.T. Lopez-Lopez, V. Carriel, In vitro characterization of a novel magnetic fibrin-agarose hydrogel for cartilage tissue engineering. J. Mech. Behav. Biomed. Mater. 104, 103619 (2020)

    Article  CAS  Google Scholar 

  118. F. Campos, A.B. Bonhome-Espinosa, J. Chato-Astrain, D. Sánchez-Porras, Ó.D. García-García, R. Carmona, M.T. López-López, M. Alaminos, V. Carriel, I.A. Rodriguez, Evaluation of fibrin-agarose tissue-like hydrogels biocompatibility for tissue engineering applications. Front. Bioeng. Biotechnol. 8, 596 (2020)

    Article  Google Scholar 

  119. S.P. Miguel, M.P. Ribeiro, H. Brancal, P. Coutinho, I.J. Correia, Thermoresponsive chitosan–agarose hydrogel for skin regeneration. Carbohyd. Polym. 111, 366–373 (2014)

    Article  CAS  Google Scholar 

  120. T. Su, M. Zhang, Q. Zeng, W. Pan, Y. Huang, Y. Qian, W. Dong, X. Qi, J. Shen, Mussel-inspired agarose hydrogel scaffolds for skin tissue engineering. Bioact. Mater. 6, 579–588 (2021)

    Article  CAS  Google Scholar 

  121. P.R. Sivashankari, M. Prabaharan, Three-dimensional porous scaffolds based on agarose/chitosan/graphene oxide composite for tissue engineering. Int. J. Biol. Macromol. 146, 222–231 (2020)

    Article  CAS  Google Scholar 

  122. D.W. Hutmacher, Scaffold design and fabrication technologies for engineering tissues–state of the art and future perspectives. J. Biomater. Sci. Polym. Ed. 12, 107–124 (2001)

    Article  CAS  Google Scholar 

  123. M.E. Gomes, A.S. Ribeiro, P.B. Malafaya, R.L. Reis, A.M. Cunha, A new approach based on injection moulding to produce biodegradable starch-based polymeric scaffolds: morphology, mechanical and degradation behaviour. Biomaterials 22, 883–889 (2001)

    Article  CAS  Google Scholar 

  124. L.P. Yan, J.M. Oliveira, A.L. Oliveira, S.G. Caridade, J.F. Mano, R.L. Reis, Macro/microporous silk fibroin scaffolds with potential for articular cartilage and meniscus tissue engineering applications. Acta Biomater. 8, 289–301 (2012)

    Article  CAS  Google Scholar 

  125. A.M. Martins, M.I. Santos, H.S. Azevedo, P.B. Malafaya, R.L. Reis, Natural origin scaffolds with in situ pore forming capability for bone tissue engineering applications. Acta Biomater. 4, 1637–1645 (2008)

    Article  CAS  Google Scholar 

  126. E.S. Miranda, T.H. Silva, R.L. Reis, J.F. Mano, Nanostructured natural-based polyelectrolyte multilayers to agglomerate chitosan particles into scaffolds for tissue engineering. Tissue Eng. Part A 17, 2663–2674 (2011)

    Article  CAS  Google Scholar 

  127. C.T. Laurencin, L.S. Nair, The quest towards limb regeneration: a regenerative engineering approach. Regen. Biomater. 3, 123–125 (2016)

    Article  Google Scholar 

  128. E.A. Phelps, A.J. Garcia, Update on therapeutic vascularization strategies. Regen. Med. 4, 65–80 (2009)

    Article  Google Scholar 

  129. S.V. Gohil, S. Brittain, H.M. Kan, H. Drissi, D. Rowe, L.S. Nair, Evaluation of enzymatically crosslinked injectable glycol chitosan gel. J. Mater. Chem. B 3, 5511–5522 (2015)

    Article  CAS  Google Scholar 

  130. W.C.L. Kenry, K.P. Loh, C.T. Lim, When stem cells meet graphene: opportunities and challenges in regenerative medicine. Biomaterials 155, 236–250 (2018)

    Article  CAS  Google Scholar 

  131. H. Jahangirian, E.G. Lemraski, R. Rafiee-Moghaddam, T.J. Webster, A review of using green chemistry methods for biomaterials in tissue engineering. Int. J. Nanomed. 13, 5953–5969 (2018)

    Article  CAS  Google Scholar 

  132. E.D. Silva, P.S. Babo, R. Costa-Almeida, R.M.A. Domingues, B.B. Mendes, E. Paz, P. Freitas, M.T. Rodrigues, P.L. Granja, M.E. Gomes, Multifunctional magnetic-responsive hydrogels to engineer tendon-to-bone interface. Nanomedicine 14, 2375–2385 (2018)

    Article  CAS  Google Scholar 

  133. P. Abdollahiyan, B. Baradaran, Mdl Guardia, F. Oroojalian, A. Mokhtarzadeh, Cutting-edge progress and challenges in stimuli responsive hydrogel microenvironment for success in tissue engineering today. J. Control. Release 328, 514–531 (2020)

    Article  CAS  Google Scholar 

  134. N. Sood, A. Bhardwaj, S. Mehta, A. Mehta, Stimuli-responsive hydrogels in drug delivery and tissue engineering. Drug Deliv. 23, 758–780 (2016)

    Article  CAS  Google Scholar 

  135. T.L. Schenck, U. Hopfner, M.N. Chávez, H.-G. Machens, I. Somlai-Schweiger, R.E. Giunta, A.V. Bohne, J. Nickelsen, M.L. Allende, J.T. Egaña, Photosynthetic biomaterials: a pathway towards autotrophic tissue engineering. Acta Biomater. 15, 39–47 (2015)

    Article  CAS  Google Scholar 

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  1. Faculty of Pharmacy and Pharmaceutical Sciences, Isfahan University of Medical Sciences, 81746-73461, Isfahan, Iran

    Siavash Iravani

  2. School of Medicine, Isfahan University of Medical Sciences, 81746-73461, Isfahan, Iran

    Ghazaleh Jamalipour Soufi

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Iravani, S., Jamalipour Soufi, G. Algae-derived materials for tissue engineering and regenerative medicine applications: current trends and future perspectives. emergent mater. 5, 631–652 (2022). https://doi.org/10.1007/s42247-021-00283-6

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