The research advances of three dimensional porous cryogel for tissue engineering_Journal of Biomedical Engineering

Authors：

LIU Shuang , XIAO Jing , CHEN Ke ,  XIAO Wenqian ,  LI Bo

Chongqing Key Laboratory of Nano/Micro Composite Materials and Devices, Chongqing University of Science and Technology, Chongqing 401331;

Corresponding author：

Keywords：

cryogel; cryopolymerization; tissue engineering; scaffold

DOI：

10.7507/1001-5515.202008057

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Cryogels are a type of hydrogel material which are fabricated by cryopolymerization at subzero temperature. Due to their unique macroporous structure, shape memory properties and injectability, cryogels have gained significant interest in the fields of tissue engineering for encouraging the repair and regeneration of injured tissues. In this review, the basic concepts relevant to cryogels are introduced, and then the fabrication principle, the process parameters and the unique properties of cryogel are discussed. Next, the latest advances of cryogels as three-dimensional scaffold for various tissue engineering applications are given. Finally, this review summarizes the current limitations of cryogels, and strategies to further improve their properties for tissue engineering. The purpose of this article is to provide a reference guide for the researchers in related fields.

Citation： LIU Shuang, XIAO Jing, CHEN Ke, XIAO Wenqian, LI Bo. The research advances of three dimensional porous cryogel for tissue engineering. Journal of Biomedical Engineering, 2021, 38(2): 393-398, 404. doi: 10.7507/1001-5515.202008057 Copy

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2.	Hollister S J. Porous scaffold design for tissue engineering. Nat Mater, 2005, 4(7): 518-524.
3.	Zhang Y S, Khademhosseini A. Advances in engineering hydrogels. Science, 2017, 356(6337): f3627.
4.	Spicer C D. Hydrogel scaffolds for tissue engineering: the importance of polymer choice. Polym Chem, 2020, 11(2): 184-219.
5.	Hixon K R, Lu T, Sell S A. A comprehensive review of cryogels and their roles in tissue engineering applications. Acta Biomater, 2017, 62: 29-41.
6.	Shah N J, Mao A S, Shih T Y, et al. An injectable bone marrow-like scaffold enhances T cell immunity after hematopoietic stem cell transplantation. Nat Biotechnol, 2019, 37(3): 293-302.
7.	Shih T Y, Blacklow S O, Li A W, et al. Injectable, tough alginate cryogels as cancer vaccines. Adv Healthc Mater, 2018, 7(10): e1701469.
8.	Im P, Kim J. On-Demand macroscale delivery system based on a macroporous cryogel with a high drug loading capacity for enhanced cancer therapy. ACS Biomater Sci Eng, 2018, 4(10): 3498-3505.
9.	Henderson T M A, Ladewig K, Haylock D N, et al. Cryogels for biomedical applications. J Mater Chem B, 2013, 1(21): 2682-2695.
10.	Okay O. Polymeric cryogels: macroporous gels with remarkable properties. New York: Springer International Publishing, 2014.
11.	Razavi M, Qiao Y, Thakor A S. Three-dimensional cryogels for biomedical applications. J Biomed Mater Res A, 2019, 107(12): 2736-2755.
12.	Kim I, Lee S S, Bae S, et al. Heparin functionalized injectable cryogel with rapid Shape-Recovery property for neovascularization. Biomacromolecules, 2018, 19(6): 2257-2269.
13.	Béduer A, Piacentini N, Aeberli L, et al. Additive manufacturing of hierarchical injectable scaffolds for tissue engineering. Acta Biomater, 2018, 76: 71-79.
14.	Eggermont L J, Rogers Z J, Colombani T, et al. Injectable cryogels for biomedical applications. Trends Biotechnol, 2020, 38(4): 418-431.
15.	Tong X, Yang F. Recent progress in developing injectable matrices for enhancing cell delivery and tissue regeneration. Adv Healthc Mater, 2018, 7(7): e1701065.
16.	Villard P, Rezaeeyazdi M, Colombani T, et al. Autoclavable and injectable cryogels for biomedical applications. Adv Healthc Mater, 2019, 8(17): e1900679.
17.	Hu W, Wang Z, Xiao Y, et al. Advances in crosslinking strategies of biomedical hydrogels. Biomater Sci, 2019, 7(3): 843-855.
18.	Serex L, Braschler T, Filippova A, et al. Pore size manipulation in 3D printed cryogels enables selective cell seeding. Adv Mater Technol, 2018, 3(4): 1700340.
19.	Memic A, Colombani T, Eggermont L J, et al. Latest advances in cryogel technology for biomedical applications. Adv Ther (Weinh), 2019, 2(4): 1800114.
20.	Koons G L, Diba M, Mikos A G. Materials design for bone-tissue engineering. Nat Rev Mater, 2020, 5(8): 584-603.
21.	Hixon K R, Eberlin C T, LU T, et al. The calcification potential of cryogel scaffolds incorporated with various forms of hydroxyapatite for bone regeneration. Biomed Mater, 2017, 12(2): 025005.
22.	Salgado C L, Grenho L, Fernandes M H, et al. Biodegradation, biocompatibility, and osteoconduction evaluation of collagen-nanohydroxyapatite cryogels for bone tissue regeneration. J Biomed Mater Res A, 2016, 104(1): 57-70.
23.	Shalumon K T, Kuo C, Wong C, et al. Gelatin/nanohyroxyapatite cryogel embedded poly(lactic-co-glycolic acid)/nanohydroxyapatite microsphere hybrid scaffolds for simultaneous bone regeneration and load-bearing. Polymers, 2018, 10(6): 620.
24.	Shalumon K T, Liao H T, Kuo C Y, et al. Rational design of gelatin/nanohydroxyapatite cryogel scaffolds for bone regeneration by introducing chemical and physical cues to enhance osteogenesis of bone marrow mesenchymal stem cells. Mater Sci Eng; C, 2019, 104: 109855.
25.	Gu L, Zhang J, Li L, et al. Hydroxyapatite nanowire composited gelatin cryogel with improved mechanical properties and cell migration for bone regeneration. Biomed Mater, 2019, 14(4): 045001.
26.	Ferreira F V, Souza L P, Martins T, et al. Nanocellulose/bioactive glass cryogels as scaffolds for bone regeneration. Nanoscale, 2019, 11(42): 19842-19849.
27.	Lee S S, Kim J H, Jeong J, et al. Sequential growth factor releasing double cryogel system for enhanced bone regeneration. Biomaterials, 2020, 257: 120223.
28.	Han M E, Kang B J, Kim S H, et al. Gelatin-based extracellular matrix cryogels for cartilage tissue engineering. Journal of Industrial and Engineering Chemistry, 2017, 45: 421-429.
29.	Jeznach O, Kołbuk D, Sajkiewicz P. Injectable hydrogels and nanocomposite hydrogels for cartilage regeneration. J Biomed Mater Res A, 2018, 106(10): 2762-2776.
30.	Liu M, Zeng X, Ma C, et al. Injectable hydrogels for cartilage and bone tissue engineering. Bone Res, 2017, 5(1): 17014.
31.	He T, Li B, Colombani T, et al. Hyaluronic acid-based shape memory cryogel scaffolds for focal cartilage defect repair. Osteoarthritis and Cartilage, 2020, 28: S504.
32.	Gupta A, Bhat S, Chaudhari B P, et al. Cell factory-derived bioactive molecules with polymeric cryogel scaffold enhance the repair of subchondral cartilage defect in rabbits. J Tissue Eng Regen Med, 2017, 11(6): 1689-1700.
33.	Zhao X, Guo B, Wu H, et al. Injectable antibacterial conductive nanocomposite cryogels with rapid shape recovery for noncompressible hemorrhage and wound healing. Nat Commun, 2018, 9(1): 2784.
34.	Li M, Zhang Z, Liang Y, et al. Multifunctional tissue-adhesive cryogel wound dressing for rapid nonpressing surface hemorrhage and wound repair. ACS Appl Mater Interfaces, 2020, 12(32): 35856-35872.
35.	Wang H M, Chou Y T, Wen Z H, et al. Novel biodegradable porous scaffold applied to skin regeneration. PLoS One, 2013, 8(6): e56330.
36.	Tyeb S, Shiekh P A, Verma V, et al. Adipose-derived stem cells (ADSCs) loaded Gelatin-Sericin-Laminin cryogels for tissue regeneration in diabetic wounds. Biomacromolecules, 2020, 21(2): 294-304.
37.	Priya S G, Gupta A, Jain E, et al. Bilayer cryogel wound dressing and skin regeneration grafts for the treatment of acute skin wounds. ACS Appl Mater Interfaces, 2016, 8(24): 15145-15159.
38.	Zeng Y, Zhu L, Han Q, et al. Preformed gelatin microcryogels as injectable cell carriers for enhanced skin wound healing. Acta Biomater, 2015, 25: 291-303.
39.	Jurga M, Dainiak M B, Sarnowska A, et al. The performance of laminin-containing cryogel scaffolds in neural tissue regeneration. Biomaterials, 2011, 32(13): 3423-3434.
40.	Béduer A, Braschler T, Peric O, et al. A compressible scaffold for minimally invasive delivery of large intact neuronal networks. Adv Healthc Mater, 2015, 4(2): 301-312.
41.	Wieringa P A, de Pinho A R G, Micera S, et al. Biomimetic architectures for peripheral nerve repair: a review of biofabrication strategies. Adv Healthc Mater, 2018, 7(8): e1701164.
42.	Singh A, Shiekh P A, Das M, et al. Aligned Chitosan-Gelatin cryogel-filled polyurethane nerve guidance channel for neural tissue engineering: fabrication, characterization, and in vitro evaluation. Biomacromolecules, 2019, 20(2): 662-673.
43.	Tao J, Hu Y, Wang S, et al. A 3D-engineered porous conduit for peripheral nerve repair. Sci Rep, 2017, 7(1): 46038.

1. Shafiee A, Atala A. Tissue engineering: toward a new era of medicine. Annu Rev Med, 2017, 68(1): 29-40.
2. Hollister S J. Porous scaffold design for tissue engineering. Nat Mater, 2005, 4(7): 518-524.
3. Zhang Y S, Khademhosseini A. Advances in engineering hydrogels. Science, 2017, 356(6337): f3627.
4. Spicer C D. Hydrogel scaffolds for tissue engineering: the importance of polymer choice. Polym Chem, 2020, 11(2): 184-219.
5. Hixon K R, Lu T, Sell S A. A comprehensive review of cryogels and their roles in tissue engineering applications. Acta Biomater, 2017, 62: 29-41.
6. Shah N J, Mao A S, Shih T Y, et al. An injectable bone marrow-like scaffold enhances T cell immunity after hematopoietic stem cell transplantation. Nat Biotechnol, 2019, 37(3): 293-302.
7. Shih T Y, Blacklow S O, Li A W, et al. Injectable, tough alginate cryogels as cancer vaccines. Adv Healthc Mater, 2018, 7(10): e1701469.
8. Im P, Kim J. On-Demand macroscale delivery system based on a macroporous cryogel with a high drug loading capacity for enhanced cancer therapy. ACS Biomater Sci Eng, 2018, 4(10): 3498-3505.
9. Henderson T M A, Ladewig K, Haylock D N, et al. Cryogels for biomedical applications. J Mater Chem B, 2013, 1(21): 2682-2695.
10. Okay O. Polymeric cryogels: macroporous gels with remarkable properties. New York: Springer International Publishing, 2014.
11. Razavi M, Qiao Y, Thakor A S. Three-dimensional cryogels for biomedical applications. J Biomed Mater Res A, 2019, 107(12): 2736-2755.
12. Kim I, Lee S S, Bae S, et al. Heparin functionalized injectable cryogel with rapid Shape-Recovery property for neovascularization. Biomacromolecules, 2018, 19(6): 2257-2269.
13. Béduer A, Piacentini N, Aeberli L, et al. Additive manufacturing of hierarchical injectable scaffolds for tissue engineering. Acta Biomater, 2018, 76: 71-79.
14. Eggermont L J, Rogers Z J, Colombani T, et al. Injectable cryogels for biomedical applications. Trends Biotechnol, 2020, 38(4): 418-431.
15. Tong X, Yang F. Recent progress in developing injectable matrices for enhancing cell delivery and tissue regeneration. Adv Healthc Mater, 2018, 7(7): e1701065.
16. Villard P, Rezaeeyazdi M, Colombani T, et al. Autoclavable and injectable cryogels for biomedical applications. Adv Healthc Mater, 2019, 8(17): e1900679.
17. Hu W, Wang Z, Xiao Y, et al. Advances in crosslinking strategies of biomedical hydrogels. Biomater Sci, 2019, 7(3): 843-855.
18. Serex L, Braschler T, Filippova A, et al. Pore size manipulation in 3D printed cryogels enables selective cell seeding. Adv Mater Technol, 2018, 3(4): 1700340.
19. Memic A, Colombani T, Eggermont L J, et al. Latest advances in cryogel technology for biomedical applications. Adv Ther (Weinh), 2019, 2(4): 1800114.
20. Koons G L, Diba M, Mikos A G. Materials design for bone-tissue engineering. Nat Rev Mater, 2020, 5(8): 584-603.
21. Hixon K R, Eberlin C T, LU T, et al. The calcification potential of cryogel scaffolds incorporated with various forms of hydroxyapatite for bone regeneration. Biomed Mater, 2017, 12(2): 025005.
22. Salgado C L, Grenho L, Fernandes M H, et al. Biodegradation, biocompatibility, and osteoconduction evaluation of collagen-nanohydroxyapatite cryogels for bone tissue regeneration. J Biomed Mater Res A, 2016, 104(1): 57-70.
23. Shalumon K T, Kuo C, Wong C, et al. Gelatin/nanohyroxyapatite cryogel embedded poly(lactic-co-glycolic acid)/nanohydroxyapatite microsphere hybrid scaffolds for simultaneous bone regeneration and load-bearing. Polymers, 2018, 10(6): 620.
24. Shalumon K T, Liao H T, Kuo C Y, et al. Rational design of gelatin/nanohydroxyapatite cryogel scaffolds for bone regeneration by introducing chemical and physical cues to enhance osteogenesis of bone marrow mesenchymal stem cells. Mater Sci Eng; C, 2019, 104: 109855.
25. Gu L, Zhang J, Li L, et al. Hydroxyapatite nanowire composited gelatin cryogel with improved mechanical properties and cell migration for bone regeneration. Biomed Mater, 2019, 14(4): 045001.
26. Ferreira F V, Souza L P, Martins T, et al. Nanocellulose/bioactive glass cryogels as scaffolds for bone regeneration. Nanoscale, 2019, 11(42): 19842-19849.
27. Lee S S, Kim J H, Jeong J, et al. Sequential growth factor releasing double cryogel system for enhanced bone regeneration. Biomaterials, 2020, 257: 120223.
28. Han M E, Kang B J, Kim S H, et al. Gelatin-based extracellular matrix cryogels for cartilage tissue engineering. Journal of Industrial and Engineering Chemistry, 2017, 45: 421-429.
29. Jeznach O, Kołbuk D, Sajkiewicz P. Injectable hydrogels and nanocomposite hydrogels for cartilage regeneration. J Biomed Mater Res A, 2018, 106(10): 2762-2776.
30. Liu M, Zeng X, Ma C, et al. Injectable hydrogels for cartilage and bone tissue engineering. Bone Res, 2017, 5(1): 17014.
31. He T, Li B, Colombani T, et al. Hyaluronic acid-based shape memory cryogel scaffolds for focal cartilage defect repair. Osteoarthritis and Cartilage, 2020, 28: S504.
32. Gupta A, Bhat S, Chaudhari B P, et al. Cell factory-derived bioactive molecules with polymeric cryogel scaffold enhance the repair of subchondral cartilage defect in rabbits. J Tissue Eng Regen Med, 2017, 11(6): 1689-1700.
33. Zhao X, Guo B, Wu H, et al. Injectable antibacterial conductive nanocomposite cryogels with rapid shape recovery for noncompressible hemorrhage and wound healing. Nat Commun, 2018, 9(1): 2784.
34. Li M, Zhang Z, Liang Y, et al. Multifunctional tissue-adhesive cryogel wound dressing for rapid nonpressing surface hemorrhage and wound repair. ACS Appl Mater Interfaces, 2020, 12(32): 35856-35872.
35. Wang H M, Chou Y T, Wen Z H, et al. Novel biodegradable porous scaffold applied to skin regeneration. PLoS One, 2013, 8(6): e56330.
36. Tyeb S, Shiekh P A, Verma V, et al. Adipose-derived stem cells (ADSCs) loaded Gelatin-Sericin-Laminin cryogels for tissue regeneration in diabetic wounds. Biomacromolecules, 2020, 21(2): 294-304.
37. Priya S G, Gupta A, Jain E, et al. Bilayer cryogel wound dressing and skin regeneration grafts for the treatment of acute skin wounds. ACS Appl Mater Interfaces, 2016, 8(24): 15145-15159.
38. Zeng Y, Zhu L, Han Q, et al. Preformed gelatin microcryogels as injectable cell carriers for enhanced skin wound healing. Acta Biomater, 2015, 25: 291-303.
39. Jurga M, Dainiak M B, Sarnowska A, et al. The performance of laminin-containing cryogel scaffolds in neural tissue regeneration. Biomaterials, 2011, 32(13): 3423-3434.
40. Béduer A, Braschler T, Peric O, et al. A compressible scaffold for minimally invasive delivery of large intact neuronal networks. Adv Healthc Mater, 2015, 4(2): 301-312.
41. Wieringa P A, de Pinho A R G, Micera S, et al. Biomimetic architectures for peripheral nerve repair: a review of biofabrication strategies. Adv Healthc Mater, 2018, 7(8): e1701164.
42. Singh A, Shiekh P A, Das M, et al. Aligned Chitosan-Gelatin cryogel-filled polyurethane nerve guidance channel for neural tissue engineering: fabrication, characterization, and in vitro evaluation. Biomacromolecules, 2019, 20(2): 662-673.
43. Tao J, Hu Y, Wang S, et al. A 3D-engineered porous conduit for peripheral nerve repair. Sci Rep, 2017, 7(1): 46038.

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The research advances of three dimensional porous cryogel for tissue engineering

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