Volume 22, Issue 3 (2019)                   mjms 2019, 22(3): 159-172 | Back to browse issues page

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Faghihi F, Khoraminia F, Imani R. Immune-Mediated Tissue Regeneration Driven by a Biomaterial Scaffold: An Innovative Regenerative Medicine Strategy. mjms. 2019; 22 (3) :159-172
URL: http://mjms.modares.ac.ir/article-30-31312-en.html
1- Biomaterial Department, Biomedical Engineering Faculty, Amirkabir University of Technology, Tehran, Iran
2- Tissue Engineering Department, Biomedical Engineering Faculty, Amirkabir University of Technology, Tehran, Iran
3- Tissue Engineering Department, Biomedical Engineering Faculty, Amirkabir University of Technology, Tehran, Iran , r.imani@aut.ac.ir
Abstract:   (5091 Views)
One of the most important applications of tissue engineering is aiding in the healing and regeneration of damaged tissues. There are many methods, which can be used to control the healing process and direct it to complete regeneration of the damaged tissue. Considering advances in the understanding of different aspects of the healing process, it is obvious that the immune system and inflammatory factors which are excreted by immune cells play an important role in complete regeneration. Actually, without the presence of the immune system, the healing process would not progress properly. Recently, the direction of researches in immunotherapy is toward using tissue engineering techniques for control and manipulation of the activity of immune cells. In this approach, implantation of biomaterials and scaffolds could be utilized for the stimulation of immune cells and secretion of different cytokines in order to improve the healing process. Biomaterial engineering approaches can manipulate and improve the effectiveness of the immune cells on tissue regeneration process via changing scaffolds surface properties (e.g. topography, roughness, crosslinking, and porosity), shape and geometry, size and surface chemistry and also providing sustainable release of cytokines and cell therapy. In this review, we focus on different aspects of the immune system effects on tissue regeneration. We also overview the tissue engineering methods for control and manipulation of the immune cells, which are participating in the healing process.
Full-Text [PDF 1412 kb]   (1914 Downloads)    
Article Type: Systematic Review | Subject: Tissue Engineering
Received: 2019/03/14 | Accepted: 2019/04/15

1. Mano JF, Silva GA, Azevedo HS, Malafaya PB, Sousa RA, Silva SS, et al. Natural origin biodegradable systems in tissue engineering and regenerative medicine: Present status and some moving trends. J R Soc Interface. 2007;4(17):999-1030. [Link] [DOI:10.1098/rsif.2007.0220]
2. Berthiaume F, Maguire TJ, Yarmush ML. Tissue engineering and regenerative medicine: History, progress, and challenges. Annu Rev Chem Biomol Eng. 2011;2:403-30. [Link] [DOI:10.1146/annurev-chembioeng-061010-114257]
3. Ma PX. Biomimetic materials for tissue engineering. Adv Drug Deliv Rev. 2008;60(2):184-98. [Link] [DOI:10.1016/j.addr.2007.08.041]
4. Sun J, Tan H. Alginate-based biomaterials for regenerative medicine applications. Materials (Basel). 2013;6(4):1285-309. [Link] [DOI:10.3390/ma6041285]
5. Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci. 2008;121(Pt 3):255-64. [Link] [DOI:10.1242/jcs.006064]
6. Andorko JI, Jewell CM. Designing biomaterials with immunomodulatory properties for tissue engineering and regenerative medicine. Bioeng Transl Med. 2017;2(2):139-55. [Link] [DOI:10.1002/btm2.10063]
7. Kopan C, Tucker T, Alexander M, Rezaa Mohammadi M, Pone EJ, Lakey JRT. Approaches in immunotherapy, regenerative medicine, and bioengineering for type 1 diabetes. Front Immunol. 2018;9:1354. [Link] [DOI:10.3389/fimmu.2018.01354]
8. Vishwakarma A, Bhise NS, Evangelista MB, Rouwkema J, Dokmeci MR, Ghaemmaghami AM, et al. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends Biotechnol. 2016;34(6):470-82. [Link] [DOI:10.1016/j.tibtech.2016.03.009]
9. Julier Z, Park AJ, Briquez PS, Martino MM. Promoting tissue regeneration by modulating the immune system. Acta Biomater. 2017;53:13-28. [Link] [DOI:10.1016/j.actbio.2017.01.056]
10. Paul WE, editor. Fundamental immunology. Philadelphia: Lippincott Williams & Wilkins; 2008. [Link]
11. Bier OG, Dias Da Silva W, Goetze D, Mota I. Fundamentals of immunology. New York: Springer Science & Business Media; 2012. [Link]
12. Abnave P, Ghigo E. Role of the immune system in regeneration and its dynamic interplay with adult stem cells. Semin Cell Dev Biol. 2019;87:160-8. [Link] [DOI:10.1016/j.semcdb.2018.04.002]
13. Michaud DS, Andres Houseman E, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. Understanding the role of the immune system in the development of cancer: New opportunities for population-based research. Cancer Epidemiol Biomark Prev. 2015;24(12):1811-9. [Link] [DOI:10.1158/1055-9965.EPI-15-0681]
14. Chang MK, Raggatt LJ, Alexander KA, Kuliwaba JS, Fazzalari NL, Schroder K, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol. 2008;181(2):1232-44. [Link] [DOI:10.4049/jimmunol.181.2.1232]
15. Van Amerongen MJ, Harmsen MC, Van Rooijen N, Petersen AH, Van Luyn MJA. Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol. 2007;170(3):818-29. [Link] [DOI:10.2353/ajpath.2007.060547]
16. Davis PA, Corless DJ, Aspinall R, Wastell C. Effect of CD4+ and CD8+ cell depletion on wound healing. Br J Surg. 2001;88(2):298-304. [Link] [DOI:10.1046/j.1365-2168.2001.01665.x]
17. Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res. 1991;(262):3-11. [Link] [DOI:10.1097/00003086-199101000-00002]
18. Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg. 2004;187(5A):11S-6. [Link] [DOI:10.1016/S0002-9610(03)00296-4]
19. Eming SA, Hammerschmidt M, Krieg T, Roers A. Interrelation of immunity and tissue repair or regeneration. Semin Cell Dev Biol. 2009;20(5):517-27. [Link] [DOI:10.1016/j.semcdb.2009.04.009]
20. Eming SA, Wynn TA, Martin P. Inflammation and metabolism in tissue repair and regeneration. Science. 2017;356(6342):1026-30. [Link] [DOI:10.1126/science.aam7928]
21. Simpson DM, Ross R. The neutrophilic leukocyte in wound repair a study with antineutrophil serum. J Clin Invest. 1972;51(8):2009-23. [Link] [DOI:10.1172/JCI107007]
22. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159-75. [Link] [DOI:10.1038/nri3399]
23. Wulff BC, Wilgus TA. Mast cell activity in the healing wound: More than meets the eye?. Exp Dermatol. 2013;22(8):507-10. [Link] [DOI:10.1111/exd.12169]
24. Szpaderska AM, Egozi EI, Gamelli RL, Di Pietro LA. The effect of thrombocytopenia on dermal wound healing. J Invest Dermatol. 2003;120(6):1130-7. [Link] [DOI:10.1016/S0022-202X(18)32320-0]
25. Leibovich SJ, Ross R. The role of the macrophage in wound repair, a study with hydrocortisone and antimacrophage serum. Am J Pathol. 1975;78(1):71-100. [Link]
26. Wynn TA, Vannella KM. Macrophages in tissue repair, regeneration, and fibrosis. Immunity. 2016;44(3):450-62. [Link] [DOI:10.1016/j.immuni.2016.02.015]
27. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453:314-21. [Link] [DOI:10.1038/nature07039]
28. Spiller KL, Nassiri S, Witherel CE, Anfang RR, Ng J, Nakazawa KR, et al. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials. 2015;37:194-207. [Link] [DOI:10.1016/j.biomaterials.2014.10.017]
29. Novak ML, Koh TJ. Macrophage phenotypes during tissue repair. J Leukoc Biol. 2013;93(6):875-81. [Link] [DOI:10.1189/jlb.1012512]
30. Bolandi B, Imani R. A sustained release gene delivery system based on polymerosome-entrapped injectable hydrogel for articular cartilage tissue engineering: A hypothetical approach. J Appl Tissue Eng. 2018;5(2). [Link]
31. Spiller KL, Koh TJ. Macrophage-based therapeutic strategies in regenerative medicine. Adv Drug Deliv Rev. 2017;122:74-83. [Link] [DOI:10.1016/j.addr.2017.05.010]
32. Fishel RS, Barbul A, Beschorner WE, Wasserkrug HL, Efron G. Lymphocyte participation in wound healing, morphologic assessment using monoclonal antibodies. Ann Surg. 1987;206(1):25-9. [Link] [DOI:10.1097/00000658-198707000-00004]
33. Efron JE, Frankel HL, Lazarou SA, Wasserkrug HL, Barbul A. Wound healing and T-lymphocytes. J Surg Res. 1990;48(5):460-3. [Link] [DOI:10.1016/0022-4804(90)90013-R]
34. Hauser CJ, Zhou X, Joshi P, Cuchens MA, Kregor P, Devidas M, et al. The immune microenvironment of human fracture/soft-tissue hematomas and its relationship to systemic immunity. J Trauma. 1997;42(5):895-903. [Link] [DOI:10.1097/00005373-199705000-00021]
35. Linfert D, Chowdhry T, Rabb H. Lymphocytes and ischemia-reperfusion injury. Transplant Rev (Orlando). 2009;23(1):1-10. [Link] [DOI:10.1016/j.trre.2008.08.003]
36. Barbul A, Shawe T, Rotter SM, Efron JE, Wasserkrug HL, Badawy SB. Wound healing in nude mice: A study on the regulatory role of lymphocytes in fibroplasia. Surgery. 1989;105(6):764-9. [Link]
37. Stout RD, Suttles J. T cell signaling of macrophage function in inflammatory disease. Front Biosci. 1997;2:d197-206. [Link] [DOI:10.2741/A183]
38. Schäffer M, Barbul A. Lymphocyte function in wound healing and following injury. Br J Surg. 1998;85(4):444-60. [Link] [DOI:10.1046/j.1365-2168.1998.00734.x]
39. Hajian M, Mahmoodi M, Imani R. In vitro assessment of poly (vinyl alcohol) film incorporating aloe vera for potential application as a wound dressing. J Macromol Sci Part B. 2017;56(7):435-50. [Link] [DOI:10.1080/00222348.2017.1330183]
40. Tsirogianni AK, Moutsopoulos NM, Moutsopoulos HM. Wound healing: Immunological aspects. Injury. 2006;37 Suppl 1:S5-12. [Link] [DOI:10.1016/j.injury.2006.02.035]
41. Wilgus TA. Immune cells in the healing skin wound: Influential players at each stage of repair. Pharmacol Res. 2008;58(2):112-6. [Link] [DOI:10.1016/j.phrs.2008.07.009]
42. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet. 2005;366(9498):1736-43. [Link] [DOI:10.1016/S0140-6736(05)67700-8]
43. De Oliveira Gonzalez AC, Costa TF, De Araújo Andrade Z, Peixoto Medrado ARA. Wound healing - a literature review. Anais Brasileiros de Dermatologia. 2016;91(5):614-20. [Link] [DOI:10.1590/abd1806-4841.20164741]
44. Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol. 2007;25(1):9-18. [Link] [DOI:10.1016/j.clindermatol.2006.09.007]
45. Assoian RK, Komoriya A, Meyers CA, Miller DM, Sporn MB. Transforming growth factor-beta in human platelets, identification of a major storage site, purification, and characterization. J Biol Chem. 1983;258(11):7155-60. [Link]
46. Greiling D, Clark RA. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci. 1997;110(Pt 7):861-70. [Link]
47. Mountziaris PM, Mikos AG. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng Part B Rev. 2008;14(2):179-86. [Link] [DOI:10.1089/ten.teb.2008.0038]
48. Meskinfam M, Bertoldi S, Albanese N, Cerri A, Tanzi MC, Imani R, et al. Polyurethane foam/nano hydroxyapatite composite as a suitable scaffold for bone tissue regeneration. Mater Sci Eng C Mater Biol Appl. 2018;82:130-40. [Link] [DOI:10.1016/j.msec.2017.08.064]
49. Chen Z, Klein T, Murray RZ, Crawford R, Chang J, Wu C, et al. Osteoimmunomodulation for the development of advanced bone biomaterials. Mater Today. 2016;19(6):304-21. [Link] [DOI:10.1016/j.mattod.2015.11.004]
50. Toben D, Schroeder I, El Khassawna T, Mehta M, Hoffmann JE, Frisch JT, et al. Fracture healing is accelerated in the absence of the adaptive immune system. J Bone Miner Res. 2011;26(1):113-24. [Link] [DOI:10.1002/jbmr.185]
51. Nam D, Mau E, Wang Y, Wright D, Silkstone D, Whetstone H, et al. T-lymphocytes enable osteoblast maturation via IL-17F during the early phase of fracture repair. PLoS One. 2012;7(6):e40044. [Link] [DOI:10.1371/journal.pone.0040044]
52. Askalonov AA, Gordienko SM, Avdyunicheva OE, Bondarenko AV, Voronkov SF. The role of T-system immunity in reparatory regeneration of the bone tissue in animals. J Hyg Epidemiol Microbiol Immunol. 1987;31(2):219-24. [Link]
53. Einhorn TA, Gerstenfeld LC. Fracture healing: Mechanisms and interventions. Nat Rev Rheumatol. 2015;11(1):45-54. [Link] [DOI:10.1038/nrrheum.2014.164]
54. Marsell R, Einhorn TA. The biology of fracture healing. Injury. 2011;42(6):551-5. [Link] [DOI:10.1016/j.injury.2011.03.031]
55. Doll BA, Sfeir C, Azari K, Holland S, Hollinger JO. Craniofacial repair. In: Lieberman JR, Friedlaender GE, editors. Bone regeneration and repair: Biology and clinical applications. Totowa: Springer Science & Business Media; 2005. pp. 337-58. [Link] [DOI:10.1385/1-59259-863-3:337]
56. Otrock ZK, Mahfouz RA, Makarem JA, Shamseddine AI. Understanding the biology of angiogenesis: Review of the most important molecular mechanisms. Blood Cells Mol Dis. 2007;39(2):212-20. [Link] [DOI:10.1016/j.bcmd.2007.04.001]
57. Zhou Y, Han Sh, Xiao L, Han P, Wang Sh, He J, et al. Accelerated host angiogenesis and immune responses by ion release from mesoporous bioactive glass. J Mater Chem B. 2018;6(20):3274-84. [Link] [DOI:10.1039/C8TB00683K]
58. Wang B, Lv X, Chen S, Li Z, Yao J, Peng X, et al. Use of heparinized bacterial cellulose based scaffold for improving angiogenesis in tissue regeneration. Carbohydr Polym. 2018;181:948-56. [Link] [DOI:10.1016/j.carbpol.2017.11.055]
59. Kwee BJ, Budina E, Najibi AJ, Mooney DJ. CD4 T-cells regulate angiogenesis and myogenesis. Biomaterials. 2018;178:109-21. [Link] [DOI:10.1016/j.biomaterials.2018.06.003]
60. Falanga V. The chronic wound: Impaired healing and solutions in the context of wound bed preparation. Blood Cells Mol Dis. 2004;32(1):88-94. [Link] [DOI:10.1016/j.bcmd.2003.09.020]
61. Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy. 2005;4(1):3-8. [Link] [DOI:10.2174/1568010053622830]
62. Demidova-Rice TN, Durham JT, Herman IM. Wound healing angiogenesis: Innovations and challenges in acute and chronic wound healing. Adv Wound Care (New Rochelle). 2012;1(1):17-22. [Link] [DOI:10.1089/wound.2011.0308]
63. Spiller KL, Freytes DO, Vunjak-Novakovic G. Macrophages modulate engineered human tissues for enhanced vascularization and healing. Ann Biomed Eng. 2015;43(3):616-27. [Link] [DOI:10.1007/s10439-014-1156-8]
64. Anderson JM, Rodriguez A, Chang DT. Foreign body reaction to biomaterials. Semin Immunol. 2008;20(2):86-100. [Link] [DOI:10.1016/j.smim.2007.11.004]
65. Wilson CJ, Clegg RE, Leavesley DI, Pearcy MJ. Mediation of biomaterial-cell interactions by adsorbed proteins: A review. Tissue Eng. 2005;11(1-2):1-18. [Link] [DOI:10.1089/ten.2005.11.1]
66. Anderson JM, Mc Nally AK. Biocompatibility of implants: Lymphocyte/macrophage interactions. Semin Immunopathol. 2011;33(3):221-33. [Link] [DOI:10.1007/s00281-011-0244-1]
67. Brown BN, Ratner BD, Goodman SB, Amar S, Badylak SF. Macrophage polarization: An opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials. 2012;33(15):3792-802. [Link] [DOI:10.1016/j.biomaterials.2012.02.034]
68. Bridges AW, García AJ. Anti-inflammatory polymeric coatings for implantable biomaterials and devices. J Diabetes Sci Technol. 2008;2(6):984-94. [Link] [DOI:10.1177/193229680800200628]
69. Blaszykowski C, Sheikh S, Thompson M. Biocompatibility and antifouling: Is there really a link?. Trends Biotechnol. 2014;32(2):61-2. [Link] [DOI:10.1016/j.tibtech.2013.11.002]
70. Gentleman E, Fredholm YC, Jell G, Lotfibakhshaiesh N, O'Donnell MD, Hill RG, et al. The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts in vitro. Biomaterials. 2010;31(14):3949-56. [Link] [DOI:10.1016/j.biomaterials.2010.01.121]
71. Tan Y, Li S, Pitt BR, Huang L. The inhibitory role of CpG immunostimulatory motifs in cationic lipid vector-mediated transgene expression in vivo. Hum Gene Ther. 1999;10(13):2153-61. [Link] [DOI:10.1089/10430349950017149]
72. Jones JA, Chang DT, Meyerson H, Colton E, Kwon IK, Matsuda T, 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):585-96. [Link] [DOI:10.1002/jbm.a.31221]
73. Veiseh O, Doloff JC, Ma M, Vegas AJ, Tam HH, Bader AR, et al. Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates. Nat Mater. 2015;14(6):643-51. [Link] [DOI:10.1038/nmat4290]
74. Shanbhag AS, Jacobs JJ, Black J, Galante JO, Glant TT. Macrophage/particle interactions: Effect of size, composition and surface area. J Biomed Mater Res. 1994;28(1):81-90. [Link] [DOI:10.1002/jbm.820280111]
75. Matlaga BF, Yasenchak LP, Salthouse TN. Tissue response to implanted polymers: The significance of sample shape. J Biomed Mater Res. 1976;10(3):391-7. [Link] [DOI:10.1002/jbm.820100308]
76. Zandstra J, Hiemstra C, Petersen AH, Zuidema J, Van Beuge MM, Rodriguez S, et al. Microsphere size influences the foreign body reaction. Eur Cell Mater. 2014;28:335-47. [Link] [DOI:10.22203/eCM.v028a23]
77. Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: Correlating particle sizes and the resultant immune responses. Expert Rev Vaccines. 2010;9(9):1095-107. [Link] [DOI:10.1586/erv.10.89]
78. Malard O, Bouler JM, Guicheux J, Heymann D, Pilet P, Coquard C, et al. Influence of biphasic calcium phosphate granulometry on bone ingrowth, ceramic resorption, and inflammatory reactions: Preliminary in vitro and in vivo study. J Biomed Mater Res. 1999;46(1):103-11. https://doi.org/10.1002/(SICI)1097-4636(199907)46:1<103::AID-JBM12>3.0.CO;2-Z [Link] [DOI:10.1002/(SICI)1097-4636(199907)46:13.0.CO;2-Z]
79. Beattie AJ, Gilbert TW, Guyot JP, Yates AJ, Badylak SF. Chemoattraction of progenitor cells by remodeling extracellular matrix scaffolds. Tissue Eng Part A. 2009;15(5):1119-25. [Link] [DOI:10.1089/ten.tea.2008.0162]
80. Brown BN, Londono R, Tottey S, Zhang L, Kukla KA, Wolf MT, et al. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater. 2012;8(3):978-87. [Link] [DOI:10.1016/j.actbio.2011.11.031]
81. Dziki JL, Wang DS, Pineda C, Sicari BM, Rausch T, Badylak SF. Solubilized extracellular matrix bioscaffolds derived from diverse source tissues differentially influence macrophage phenotype. J Biomed Mater Res A. 2017;105(1):138-47. [Link] [DOI:10.1002/jbm.a.35894]
82. Kelly SH, Shores LS, Votaw NL, Collier JH. Biomaterial strategies for generating therapeutic immune responses. Adv Drug Deliv Rev. 2017;114:3-18. [Link] [DOI:10.1016/j.addr.2017.04.009]
83. Christian DA, Hunter CA. Particle-mediated delivery of cytokines for immunotherapy. Immunotherapy. 2012;4(4):425-41. [Link] [DOI:10.2217/imt.12.26]
84. Siebert S, Tsoukas A, Robertson J, McInnes I. Cytokines as therapeutic targets in rheumatoid arthritis and other inflammatory diseases. Pharmacol Rev. 2015;67(2):280-309. [Link] [DOI:10.1124/pr.114.009639]
85. Andorko JI, Hess KL, Pineault KG, Jewell CM. Intrinsic immunogenicity of rapidly-degradable polymers evolves during degradation. Acta Biomater. 2016;32:24-34. [Link] [DOI:10.1016/j.actbio.2015.12.026]
86. Boehler RM, Graham JG, Shea LD. Tissue engineering tools for modulation of the immune response. Biotechniques. 2011;51(4):239-40,242,244 passim. [Link] [DOI:10.2144/000113754]
87. Hume PS, He J, Haskins K, Anseth KS. Strategies to reduce dendritic cell activation through functional biomaterial design. Biomaterials. 2012;33(14):3615-25. [Link] [DOI:10.1016/j.biomaterials.2012.02.009]
88. Boehler RM, Kuo R, Shin S, Goodman AG, Pilecki MA, Leonard JN, et al. Lentivirus delivery of IL-10 to promote and sustain macrophage polarization towards an anti-inflammatory phenotype. Biotechnol Bioeng. 2014;111(6):1210-21. [Link] [DOI:10.1002/bit.25175]
89. Tsianakas A, Varga G, Barczyk K, Bode G, Nippe N, Kran N, et al. Induction of an anti-inflammatory human monocyte subtype is a unique property of glucocorticoids, but can be modified by IL-6 and IL-10. Immunobiology. 2012;217(3):329-35. [Link] [DOI:10.1016/j.imbio.2011.10.002]
90. Patil SD, Papadmitrakopoulos F, Burgess DJ. Concurrent delivery of dexamethasone and VEGF for localized inflammation control and angiogenesis. J Control Release. 2007;117(1):68-79. [Link] [DOI:10.1016/j.jconrel.2006.10.013]
91. Richardson TP, Peters MC, Ennett AB, Mooney DJ. Polymeric system for dual growth factor delivery. Nat Biotechnol. 2001;19(11):1029-34. [Link] [DOI:10.1038/nbt1101-1029]
92. Schultz GS, Wysocki A. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen. 2009;17(2):153-62. [Link] [DOI:10.1111/j.1524-475X.2009.00466.x]
93. Hynes RO. The extracellular matrix: Not just pretty fibrils. Science. 2009;326(5957):1216-9. [Link] [DOI:10.1126/science.1176009]
94. Chen S, Jones JA, Xu Y, Low HY, Anderson JM, Leong KW. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials. 2010;31(13):3479-91. [Link] [DOI:10.1016/j.biomaterials.2010.01.074]
95. Jeon H, Tsui JH, Jang SI, Lee JH, Park S, Mun K, et al. Combined effects of substrate topography and stiffness on endothelial cytokine and chemokine secretion. ACS Appl Mater Interfaces. 2015;7(8):4525-32. [Link] [DOI:10.1021/acsami.5b00554]
96. Bota PC, Collie AM, Puolakkainen P, Vernon RB, Sage EH, Ratner BD, et al. Biomaterial topography alters healing in vivo and monocyte/macrophage activation in vitro. J Biomed Mater Res A. 2010;95(2):649-57. [Link] [DOI:10.1002/jbm.a.32893]
97. Takebe J, Champagne CM, Offenbacher S, Ishibashi K, Cooper LF. Titanium surface topography alters cell shape and modulates bone morphogenetic protein 2 expression in the J774A.1 macrophage cell line. J Biomed Mater Res A. 2003;64(2):207-16. [Link] [DOI:10.1002/jbm.a.10275]
98. Mendonça G, Mendonça DB, Aragão FJ, Cooper LF. Advancing dental implant surface technology--from micron- to nanotopography. Biomaterials. 2008;29(28):3822-35. [Link] [DOI:10.1016/j.biomaterials.2008.05.012]
99. Badylak SF, Valentin JE, Ravindra AK, Mc Cabe GP, Stewart-Akers AM. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng Part A. 2008;14(11):1835-42. [Link] [DOI:10.1089/ten.tea.2007.0264]
100. Laschke MW, Harder Y, Amon M, Martin I, Farhadi J, Ring A, et al. Angiogenesis in tissue engineering: Breathing life into constructed tissue substitutes. Tissue Eng. 2006;12(8):2093-104. [Link] [DOI:10.1089/ten.2006.12.2093]
101. Klinge U, Klosterhalfen B, Birkenhauer V, Junge K, Conze J, Schumpelick V. Impact of polymer pore size on the interface scar formation in a rat model. J Surg Res. 2002;103(2):208-14. [Link] [DOI:10.1006/jsre.2002.6358]
102. Imani R, Hojjati Emami Sh, Rahnama Moshtagh P, Baheiraei N, Sharifi AM. Preparation and characterization of agarose-gelatin blend hydrogels as a cell encapsulation matrix: An in-vitro study. J Macromol Sci Part B. 2012;51(8):1606-16. [Link] [DOI:10.1080/00222348.2012.657110]
103. Rahnamay Moshtagh P, Imani R, Hojjati Emami Sh, Sharifi AM. An optimized calcium alginate microcapsule for mesenchymal stem cells encapsulation. J Appl Tissue Eng. 2018;5(1). [Link]
104. Dohle E, Bischoff I, Böse T, Marsano A, Banfi A, Unger RE, et al. Macrophage-mediated angiogenic activation of outgrowth endothelial cells in co-culture with primary osteoblasts. Eur Cell Mater. 2014;27:149-64. [Link] [DOI:10.22203/eCM.v027a12]
105. Rybalko V, Hsieh PL, Merscham-Banda M, Suggs LJ, Farrar RP. The development of macrophage-mediated cell therapy to improve skeletal muscle function after injury. PLoS One. 2015;10(12):e0145550. [Link] [DOI:10.1371/journal.pone.0145550]
106. Novak ML, Weinheimer-Haus EM, Koh TJ. Macrophage activation and skeletal muscle healing following traumatic injury. J Pathol. 2014;232(3):344-55. [Link] [DOI:10.1002/path.4301]
107. Wang Y, Wang YP, Zheng G, Lee VW, Ouyang L, Chang DH, et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int. 2007;72(3):290-9. [Link] [DOI:10.1038/sj.ki.5002275]
108. Zuloff-Shani A, Adunsky A, Even-Zahav A, Semo H, Orenstein A, Tamir J, et al. Hard to heal pressure ulcers (stage III-IV): Efficacy of injected Activated Macrophage Suspension (AMS) as compared with Standard of Care (SOC) treatment controlled trial. Arch Gerontol Geriatr. 2010;51(3):268-72. [Link] [DOI:10.1016/j.archger.2009.11.015]
109. Brunck ME, Nielsen LK. Concise review: Next-generation cell therapies to prevent infections in neutropenic patients. Stem Cells Transl Med. 2014;3(4):541-8. [Link] [DOI:10.5966/sctm.2013-0145]

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