Bone/cartilage immunomodulating hydrogels: construction strategies and applications_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Maoyuan ^1,2 , ZHENG Guoshuang ² , YANG Jiahui ² , CHEN Xiaofang ^1,2 , XU Jianfeng ^1,2 ,  ZHAO Dewei ²

1. Zhongshan Clinical College of Dalian University, Dalian Liaoning, 116001, P. R. China;
2. Department of Orthopaedics, Zhongshan Hospital, Dalian University, Dalian Liaoning, 116001, P. R. China;

Corresponding author：

ZHAO Dewei, Email: zhaodewei2000@163.com

Keywords：

Bone/cartilage tissue engineering; immunomodulation; hydrogel; construction strategy

DOI：

10.7507/1002-1892.202305081

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress in the construction strategy and application of bone/cartilage immunomodulating hydrogels. Methods The literature related to bone/cartilage immunomodulating hydrogels at home and abroad in recent years was reviewed and summarized from the immune response mechanism of different immune cells, the construction strategy of immunomodulating hydrogels, and their practical applications. Results According to the immune response mechanism of different immune cells, the biological materials with immunoregulatory effect is designed, which can regulate the immune response of the body and thus promote the regeneration of bone/cartilage tissue. Immunomodulating hydrogels have good biocompatibility, adjustability, and multifunctionality. By regulating the physical and chemical properties of hydrogel and loading factors or cells, the immune system of the body can be purposively regulated, thus forming an immune microenvironment conducive to osteochondral regeneration. Conclusion Immunomodulating hydrogels can promote osteochondral repair by affecting the immunomodulation process of host organs or cells. It has shown a wide application prospect in the repair of osteochondral defects. However, more data support from basic and clinical experiments is needed for this material to further advance its clinical translation process.

Citation： LI Maoyuan, ZHENG Guoshuang, YANG Jiahui, CHEN Xiaofang, XU Jianfeng, ZHAO Dewei. Bone/cartilage immunomodulating hydrogels: construction strategies and applications. Chinese Journal of Reparative and Reconstructive Surgery, 2023, 37(11): 1423-1430. doi: 10.7507/1002-1892.202305081 Copy

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2.	Salati MA, Khazai J, Tahmuri AM, et al. Agarose-based biomaterials: opportunities and challenges in cartilage tissue engineering. Polymers (Basel), 2020, 12(5): 1150.
3.	Saberi A, Jabbari F, Zarrintaj P, et al. Electrically conductive materials: opportunities and challenges in tissue engineering. Biomolecules, 2019, 9(9): 448.
4.	Zhang B, Su Y, Zhou J, et al. Toward a better regeneration through implant-mediated immunomodulation: harnessing the immune responses. Adv Sci (Weinh), 2021, 8(16): e2100446.
5.	Su N, Villicana C, Yang F. Immunomodulatory strategies for bone regeneration: A review from the perspective of disease types. Biomaterials, 2022, 286: 121604.
6.	Wu CL, Harasymowicz NS, Klimak MA, et al. The role of macrophages in osteoarthritis and cartilage repair. Osteoarthritis Cartilage, 2020, 28(5): 544-554.
7.	Chisari E, Yaghmour KM, Khan WS. The effects of TNF-alpha inhibition on cartilage: a systematic review of preclinical studies. Osteoarthritis Cartilage, 2020, 28(5): 708-718.
8.	Mei Q, Rao J, Bei HP, et al. 3D bioprinting photo-crosslinkable hydrogels for bone and cartilage repair. Int J Bioprint, 2021, 7(3): 367.
9.	Babaniamansour P, Salimi M, Dorkoosh F, et al. Magnetic hydrogel for cartilage tissue regeneration as well as a review on advantages and disadvantages of different cartilage repair strategies. Biomed Res Int, 2022, 2022: 7230354.
10.	Szychlinska MA, D’Amora U, Ravalli S, et al. Functional biomolecule delivery systems and bioengineering in cartilage regeneration. Curr Pharm Biotechnol, 2019, 20(1): 32-46.
11.	Bagheri B, Zarrintaj P, Surwase SS, et al. Self-gelling electroactive hydrogels based on chitosan-aniline oligomers/agarose for neural tissue engineering with on-demand drug release. Colloids Surf B Biointerfaces, 2019, 184: 110549.
12.	Xue X, Hu Y, Wang S, et al. Fabrication of physical and chemical crosslinked hydrogels for bone tissue engineering. Bioact Mater, 2021, 12: 327-339.
13.	Franz S, Rammelt S, Scharnweber D, et al. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692-6709.
14.	Heydari P, Kharaziha M, Varshosaz J, et al. Current knowledge of immunomodulation strategies for chronic skin wound repair. J Biomed Mater Res B Appl Biomater, 2022, 110(2): 265-288.
15.	Arneth B. Trained innate immunity. Immunol Res, 2021, 69(1): 1-7.
16.	Podaru MN, Fields L, Kainuma S, et al. Reparative macrophage transplantation for myocardial repair: a refinement of bone marrow mononuclear cell-based therapy. Basic Res Cardiol, 2019, 114(5): 34.
17.	Selders GS, Fetz AE, Radic MZ, et al. An overview of the role of neutrophils in innate immunity, inflammation and host-biomaterial integration. Regen Biomater, 2017, 4(1): 55-68.
18.	Branzk N, Lubojemska A, Hardison SE, et al. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol, 2014, 15(11): 1017-1025.
19.	Li X, Guan Y, Li C, et al. Immunomodulatory effects of mesenchymal stem cells in peripheral nerve injury. Stem Cell Res Ther, 2022, 13(1): 18.
20.	Ino Y, Yamazaki-Itoh R, Shimada K, et al. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer, 2013, 108(4): 914-923.
21.	Ardi VC, Kupriyanova TA, Deryugina EI, et al. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci U S A, 2007, 104(51): 20262-20267.
22.	Li W, Hsiao HM, Higashikubo R, et al. Heart-resident CCR2+ macrophages promote neutrophil extravasation through TLR9/MyD88/CXCL5 signaling. JCI Insight, 2016, 1(12): e87315.
23.	Tecchio C, Micheletti A, Cassatella MA. Neutrophil-derived cytokines: facts beyond expression. Front Immunol, 2014, 5: 508.
24.	Gomez Perdiguero E, Klapproth K, Schulz C, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature, 2015, 518(7540): 547-551.
25.	Jones JA, Chang DT, Meyerson H, et al. Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. J Biomed Mater Res A, 2007, 83(3): 585-596.
26.	Broughton G, Janis JE, Attinger CE. The basic science of wound healing. Plast Reconstr Surg, 2006, 117(7 Suppl): 12S-34S.
27.	Mantovani A, Sica A, Sozzani S, et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol, 2004, 25(12): 677-686.
28.	Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 2008, 8(12): 958-969.
29.	Wynn TA, Vannella KM. Macrophages in tissue repair, regeneration, and fibrosis. Immunity, 2016, 44(3): 450-462.
30.	Rahmati M, Silva EA, Reseland JE, et al. Biological responses to physicochemical properties of biomaterial surface. Chem Soc Rev, 2020, 49(15): 5178-5224.
31.	Vassey MJ, Figueredo GP, Scurr DJ, et al. Immune modulation by design: using topography to control human monocyte attachment and macrophage differentiation. Adv Sci (Weinh), 2020, 7(11): 1903392.
32.	Raphael I, Nalawade S, Eagar TN, et al. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine, 2015, 74(1): 5-17.
33.	Zhang DH, Chen Q, Chao S, et al. , Dealing with the foreign-body response to implanted biomaterials: strategies and applications of new materials. Advanced Functional Materials, 2021, 31(6): 2007226.
34.	Li J, Tan J, Martino MM, et al. Regulatory T-cells: Potential regulator of tissue repair and regeneration. Front Immunol, 2018, 9: 585.
35.	Stashenko P, Gonçalves RB, Lipkin B, et al. Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol, 2007, 170(1): 203-213.
36.	Desvergne B. PPARdelta/beta: the lobbyist switching macrophage allegiance in favor of metabolism. Cell Metab, 2008, 7(6): 467-469.
37.	Carbone F, Nencioni A, Mach F, et al. Pathophysiological role of neutrophils in acute myocardial infarction. Thromb Haemost, 2013, 110(3): 501-514.
38.	Li CM, Guo CC, Fitzpatrick V, et al. Design of biodegradable, implantable devices towards clinical translation. Nature Reviews Materials, 2020, 5(1): 61-81.
39.	Hsu RJ, Yu WC, Peng GR, et al. The role of cytokines and chemokines in severe acute respiratory syndrome coronavirus 2 infections. Front Immunol, 2022, 13: 832394.
40.	Cao H, Duan L, Zhang Y, et al. Current hydrogel advances in physicochemical and biological response-driven biomedical application diversity. Signal Transduct Target Ther, 2021, 6(1): 426.
41.	Elsayed MM. Hydrogel preparation technologies: relevance kinetics, thermodynamics and scaling up aspects. J Polym Environ, 2019, 27(4): 871-891.
42.	Oakes PW, Patel DC, Morin NA, et al. Neutrophil morphology and migration are affected by substrate elasticity. Blood, 2009, 114(7): 1387-1395.
43.	Jannat RA, Dembo M, Hammer DA. Traction forces of neutrophils migrating on compliant substrates. Biophys J, 2011, 101(3): 575-584.
44.	Zhuang Z, Zhang Y, Sun S, et al. Control of matrix stiffness using methacrylate-gelatin hydrogels for a macrophage-mediated inflammatory response. ACS Biomater Sci Eng, 2020, 6(5): 3091-3102.
45.	Sridharan R, Cavanagh B, Cameron AR, et al. Material stiffness influences the polarization state, function and migration mode of macrophages. Acta Biomater, 2019, 89: 47-59.
46.	Li Z, Bratlie KM. How cross-linking mechanisms of methacrylated gellan gum hydrogels alter macrophage phenotype. ACS Appl Bio Mater, 2019, 2(1): 217-225.
47.	He XT, Wu RX, Xu XY, et al. Macrophage involvement affects matrix stiffness-related influences on cell osteogenesis under three-dimensional culture conditions. Acta Biomater, 2018, 71: 132-147.
48.	Saitakis M, Dogniaux S, Goudot C, et al. Different TCR-induced T lymphocyte responses are potentiated by stiffness with variable sensitivity. Elife, 2017, 6: e23190.
49.	Pearce EL, Poffenberger MC, Chang CH, et al. Fueling immunity: insights into metabolism and lymphocyte function. Science, 2013, 342(6155): 1242454.
50.	Haeger A, Krause M, Wolf K, et al. Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. Biochim Biophys Acta, 2014, 1840(8): 2386-2395.
51.	Moshaverinia A, Chen C, Xu X, et al. Regulation of the stem cell-host immune system interplay using hydrogel coencapsulation system with an anti-inflammatory drug. Adv Funct Mater, 2015, 25(15): 2296-2307.
52.	Li X, Cho B, Martin R, et al. Nanofiber-hydrogel composite-mediated angiogenesis for soft tissue reconstruction. Sci Transl Med, 2019, 11(490): eaau6210.
53.	Singh S, Awuah D, Rostam HM, et al. Unbiased analysis of the impact of micropatterned biomaterials on macrophage behavior provides insights beyond predefined polarization states. ACS Biomater Sci Eng, 2017, 3(6): 969-978.
54.	Chen Z, Bachhuka A, Han S, et al. Tuning chemistry and topography of nanoengineered surfaces to manipulate immune response for bone regeneration applications. ACS Nano, 2017, 11(5): 4494-4506.
55.	Xu ZH, Hwang DG, Bartlett MD, et al. Alter macrophage adhesion and modulate their response on hydrophobically modified hydrogels. Biochemical Engineering Journal, 2021. doi: 10.1016/j.bej.2020.107821.
56.	da Silva Domingues JF, Roest S, Wang Y, et al. Macrophage phagocytic activity toward adhering staphylococci on cationic and patterned hydrogel coatings versus common biomaterials. Acta Biomater, 2015, 18: 1-8.
57.	Samavedi S, Whittington AR, Goldstein AS. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomater, 2013, 9(9): 8037-8045.
58.	Zhang J, Zhu Y, Song J, et al. Novel balanced charged alginate/PEI polyelectrolyte hydrogel that resists foreign-body reaction. ACS Appl Mater Interfaces, 2018, 10(8): 6879-6886.
59.	Lopez-Silva TL, Leach DG, Azares A, et al. Chemical functionality of multidomain peptide hydrogels governs early host immune response. Biomaterials, 2020, 231: 119667.
60.	Li C, Wang K, Zhou X, et al. Controllable fabrication of hydroxybutyl chitosan/oxidized chondroitin sulfate hydrogels by 3D bioprinting technique for cartilage tissue engineering. Biomed Mater, 2019, 14(2): 025006.
61.	Kim MG, Kang TW, Park JY, et al. An injectable cationic hydrogel electrostatically interacted with BMP2 to enhance in vivo osteogenic differentiation of human turbinate mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl, 2019, 103: 109853.
62.	Li BE, Zhang L, Wang DH, et al. Thermo-sensitive hydrogel on anodized titanium surface to regulate immune response. Surface & Coatings Technology, 2021, 126624.
63.	Ji X, Shao H, Li X, et al. Injectable immunomodulation-based porous chitosan microspheres/HPCH hydrogel composites as a controlled drug delivery system for osteochondral regeneration. Biomaterials, 2022, 285: 121530.
64.	Li Z, Wang H, Zhang K, et al. Bisphosphonate-based hydrogel mediates biomimetic negative feedback regulation of osteoclastic activity to promote bone regeneration. Bioact Mater, 2021, 13: 9-22.
65.	Yang M, Zhang ZC, Yuan FZ, et al. An immunomodulatory polypeptide hydrogel for osteochondral defect repair. Bioact Mater, 2022, 19: 678-689.

1. Li M, Yin H, Yan Z, et al. The immune microenvironment in cartilage injury and repair. Acta Biomater, 2022, 140: 23-42.
2. Salati MA, Khazai J, Tahmuri AM, et al. Agarose-based biomaterials: opportunities and challenges in cartilage tissue engineering. Polymers (Basel), 2020, 12(5): 1150.
3. Saberi A, Jabbari F, Zarrintaj P, et al. Electrically conductive materials: opportunities and challenges in tissue engineering. Biomolecules, 2019, 9(9): 448.
4. Zhang B, Su Y, Zhou J, et al. Toward a better regeneration through implant-mediated immunomodulation: harnessing the immune responses. Adv Sci (Weinh), 2021, 8(16): e2100446.
5. Su N, Villicana C, Yang F. Immunomodulatory strategies for bone regeneration: A review from the perspective of disease types. Biomaterials, 2022, 286: 121604.
6. Wu CL, Harasymowicz NS, Klimak MA, et al. The role of macrophages in osteoarthritis and cartilage repair. Osteoarthritis Cartilage, 2020, 28(5): 544-554.
7. Chisari E, Yaghmour KM, Khan WS. The effects of TNF-alpha inhibition on cartilage: a systematic review of preclinical studies. Osteoarthritis Cartilage, 2020, 28(5): 708-718.
8. Mei Q, Rao J, Bei HP, et al. 3D bioprinting photo-crosslinkable hydrogels for bone and cartilage repair. Int J Bioprint, 2021, 7(3): 367.
9. Babaniamansour P, Salimi M, Dorkoosh F, et al. Magnetic hydrogel for cartilage tissue regeneration as well as a review on advantages and disadvantages of different cartilage repair strategies. Biomed Res Int, 2022, 2022: 7230354.
10. Szychlinska MA, D’Amora U, Ravalli S, et al. Functional biomolecule delivery systems and bioengineering in cartilage regeneration. Curr Pharm Biotechnol, 2019, 20(1): 32-46.
11. Bagheri B, Zarrintaj P, Surwase SS, et al. Self-gelling electroactive hydrogels based on chitosan-aniline oligomers/agarose for neural tissue engineering with on-demand drug release. Colloids Surf B Biointerfaces, 2019, 184: 110549.
12. Xue X, Hu Y, Wang S, et al. Fabrication of physical and chemical crosslinked hydrogels for bone tissue engineering. Bioact Mater, 2021, 12: 327-339.
13. Franz S, Rammelt S, Scharnweber D, et al. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692-6709.
14. Heydari P, Kharaziha M, Varshosaz J, et al. Current knowledge of immunomodulation strategies for chronic skin wound repair. J Biomed Mater Res B Appl Biomater, 2022, 110(2): 265-288.
15. Arneth B. Trained innate immunity. Immunol Res, 2021, 69(1): 1-7.
16. Podaru MN, Fields L, Kainuma S, et al. Reparative macrophage transplantation for myocardial repair: a refinement of bone marrow mononuclear cell-based therapy. Basic Res Cardiol, 2019, 114(5): 34.
17. Selders GS, Fetz AE, Radic MZ, et al. An overview of the role of neutrophils in innate immunity, inflammation and host-biomaterial integration. Regen Biomater, 2017, 4(1): 55-68.
18. Branzk N, Lubojemska A, Hardison SE, et al. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol, 2014, 15(11): 1017-1025.
19. Li X, Guan Y, Li C, et al. Immunomodulatory effects of mesenchymal stem cells in peripheral nerve injury. Stem Cell Res Ther, 2022, 13(1): 18.
20. Ino Y, Yamazaki-Itoh R, Shimada K, et al. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer, 2013, 108(4): 914-923.
21. Ardi VC, Kupriyanova TA, Deryugina EI, et al. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci U S A, 2007, 104(51): 20262-20267.
22. Li W, Hsiao HM, Higashikubo R, et al. Heart-resident CCR2+ macrophages promote neutrophil extravasation through TLR9/MyD88/CXCL5 signaling. JCI Insight, 2016, 1(12): e87315.
23. Tecchio C, Micheletti A, Cassatella MA. Neutrophil-derived cytokines: facts beyond expression. Front Immunol, 2014, 5: 508.
24. Gomez Perdiguero E, Klapproth K, Schulz C, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature, 2015, 518(7540): 547-551.
25. Jones JA, Chang DT, Meyerson H, et al. Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. J Biomed Mater Res A, 2007, 83(3): 585-596.
26. Broughton G, Janis JE, Attinger CE. The basic science of wound healing. Plast Reconstr Surg, 2006, 117(7 Suppl): 12S-34S.
27. Mantovani A, Sica A, Sozzani S, et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol, 2004, 25(12): 677-686.
28. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol, 2008, 8(12): 958-969.
29. Wynn TA, Vannella KM. Macrophages in tissue repair, regeneration, and fibrosis. Immunity, 2016, 44(3): 450-462.
30. Rahmati M, Silva EA, Reseland JE, et al. Biological responses to physicochemical properties of biomaterial surface. Chem Soc Rev, 2020, 49(15): 5178-5224.
31. Vassey MJ, Figueredo GP, Scurr DJ, et al. Immune modulation by design: using topography to control human monocyte attachment and macrophage differentiation. Adv Sci (Weinh), 2020, 7(11): 1903392.
32. Raphael I, Nalawade S, Eagar TN, et al. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine, 2015, 74(1): 5-17.
33. Zhang DH, Chen Q, Chao S, et al. , Dealing with the foreign-body response to implanted biomaterials: strategies and applications of new materials. Advanced Functional Materials, 2021, 31(6): 2007226.
34. Li J, Tan J, Martino MM, et al. Regulatory T-cells: Potential regulator of tissue repair and regeneration. Front Immunol, 2018, 9: 585.
35. Stashenko P, Gonçalves RB, Lipkin B, et al. Th1 immune response promotes severe bone resorption caused by Porphyromonas gingivalis. Am J Pathol, 2007, 170(1): 203-213.
36. Desvergne B. PPARdelta/beta: the lobbyist switching macrophage allegiance in favor of metabolism. Cell Metab, 2008, 7(6): 467-469.
37. Carbone F, Nencioni A, Mach F, et al. Pathophysiological role of neutrophils in acute myocardial infarction. Thromb Haemost, 2013, 110(3): 501-514.
38. Li CM, Guo CC, Fitzpatrick V, et al. Design of biodegradable, implantable devices towards clinical translation. Nature Reviews Materials, 2020, 5(1): 61-81.
39. Hsu RJ, Yu WC, Peng GR, et al. The role of cytokines and chemokines in severe acute respiratory syndrome coronavirus 2 infections. Front Immunol, 2022, 13: 832394.
40. Cao H, Duan L, Zhang Y, et al. Current hydrogel advances in physicochemical and biological response-driven biomedical application diversity. Signal Transduct Target Ther, 2021, 6(1): 426.
41. Elsayed MM. Hydrogel preparation technologies: relevance kinetics, thermodynamics and scaling up aspects. J Polym Environ, 2019, 27(4): 871-891.
42. Oakes PW, Patel DC, Morin NA, et al. Neutrophil morphology and migration are affected by substrate elasticity. Blood, 2009, 114(7): 1387-1395.
43. Jannat RA, Dembo M, Hammer DA. Traction forces of neutrophils migrating on compliant substrates. Biophys J, 2011, 101(3): 575-584.
44. Zhuang Z, Zhang Y, Sun S, et al. Control of matrix stiffness using methacrylate-gelatin hydrogels for a macrophage-mediated inflammatory response. ACS Biomater Sci Eng, 2020, 6(5): 3091-3102.
45. Sridharan R, Cavanagh B, Cameron AR, et al. Material stiffness influences the polarization state, function and migration mode of macrophages. Acta Biomater, 2019, 89: 47-59.
46. Li Z, Bratlie KM. How cross-linking mechanisms of methacrylated gellan gum hydrogels alter macrophage phenotype. ACS Appl Bio Mater, 2019, 2(1): 217-225.
47. He XT, Wu RX, Xu XY, et al. Macrophage involvement affects matrix stiffness-related influences on cell osteogenesis under three-dimensional culture conditions. Acta Biomater, 2018, 71: 132-147.
48. Saitakis M, Dogniaux S, Goudot C, et al. Different TCR-induced T lymphocyte responses are potentiated by stiffness with variable sensitivity. Elife, 2017, 6: e23190.
49. Pearce EL, Poffenberger MC, Chang CH, et al. Fueling immunity: insights into metabolism and lymphocyte function. Science, 2013, 342(6155): 1242454.
50. Haeger A, Krause M, Wolf K, et al. Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinement. Biochim Biophys Acta, 2014, 1840(8): 2386-2395.
51. Moshaverinia A, Chen C, Xu X, et al. Regulation of the stem cell-host immune system interplay using hydrogel coencapsulation system with an anti-inflammatory drug. Adv Funct Mater, 2015, 25(15): 2296-2307.
52. Li X, Cho B, Martin R, et al. Nanofiber-hydrogel composite-mediated angiogenesis for soft tissue reconstruction. Sci Transl Med, 2019, 11(490): eaau6210.
53. Singh S, Awuah D, Rostam HM, et al. Unbiased analysis of the impact of micropatterned biomaterials on macrophage behavior provides insights beyond predefined polarization states. ACS Biomater Sci Eng, 2017, 3(6): 969-978.
54. Chen Z, Bachhuka A, Han S, et al. Tuning chemistry and topography of nanoengineered surfaces to manipulate immune response for bone regeneration applications. ACS Nano, 2017, 11(5): 4494-4506.
55. Xu ZH, Hwang DG, Bartlett MD, et al. Alter macrophage adhesion and modulate their response on hydrophobically modified hydrogels. Biochemical Engineering Journal, 2021. doi: 10.1016/j.bej.2020.107821.
56. da Silva Domingues JF, Roest S, Wang Y, et al. Macrophage phagocytic activity toward adhering staphylococci on cationic and patterned hydrogel coatings versus common biomaterials. Acta Biomater, 2015, 18: 1-8.
57. Samavedi S, Whittington AR, Goldstein AS. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomater, 2013, 9(9): 8037-8045.
58. Zhang J, Zhu Y, Song J, et al. Novel balanced charged alginate/PEI polyelectrolyte hydrogel that resists foreign-body reaction. ACS Appl Mater Interfaces, 2018, 10(8): 6879-6886.
59. Lopez-Silva TL, Leach DG, Azares A, et al. Chemical functionality of multidomain peptide hydrogels governs early host immune response. Biomaterials, 2020, 231: 119667.
60. Li C, Wang K, Zhou X, et al. Controllable fabrication of hydroxybutyl chitosan/oxidized chondroitin sulfate hydrogels by 3D bioprinting technique for cartilage tissue engineering. Biomed Mater, 2019, 14(2): 025006.
61. Kim MG, Kang TW, Park JY, et al. An injectable cationic hydrogel electrostatically interacted with BMP2 to enhance in vivo osteogenic differentiation of human turbinate mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl, 2019, 103: 109853.
62. Li BE, Zhang L, Wang DH, et al. Thermo-sensitive hydrogel on anodized titanium surface to regulate immune response. Surface & Coatings Technology, 2021, 126624.
63. Ji X, Shao H, Li X, et al. Injectable immunomodulation-based porous chitosan microspheres/HPCH hydrogel composites as a controlled drug delivery system for osteochondral regeneration. Biomaterials, 2022, 285: 121530.
64. Li Z, Wang H, Zhang K, et al. Bisphosphonate-based hydrogel mediates biomimetic negative feedback regulation of osteoclastic activity to promote bone regeneration. Bioact Mater, 2021, 13: 9-22.
65. Yang M, Zhang ZC, Yuan FZ, et al. An immunomodulatory polypeptide hydrogel for osteochondral defect repair. Bioact Mater, 2022, 19: 678-689.

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