Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Decellularized Matrices for the Treatment of Tissue Defects: from Matrix Origin to Immunological Mechanisms

  • Xinyue Wang (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Jiqiang Guo (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Qing Yu (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Luyao Zhao (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Xiang Gao (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Li Wang (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Meiling Wen (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Junrong Yan (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Meiwen An (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology) ;
  • Yang Liu (Institute of Biomedical Engineering, College of Biomedical Engineering, Taiyuan University of Technology)
  • Received : 2024.03.23
  • Accepted : 2024.05.31
  • Published : 2024.09.01
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Abstract

Decellularized matrix transplantation has emerged as a promising therapeutic approach for repairing tissue defects, with numerous studies assessing its safety and efficacy in both animal models and clinical settings. The host immune response elicited by decellularized matrix grafts of natural biological origin plays a crucial role in determining the success of tissue repair, influenced by matrix heterogeneity and the inflammatory microenvironment of the wound. However, the specific immunologic mechanisms underlying the interaction between decellularized matrix grafts and the host immune system remain elusive. This article reviews the sources of decellularized matrices, available decellularization techniques, and residual immunogenic components. It focuses on the host immune response following decellularized matrix transplantation, with emphasis on the key mechanisms of Toll-like receptor, T-cell receptor, and TGF-β/SMAD signaling in the stages of post-transplantation immunorecognition, immunomodulation, and tissue repair, respectively. Furthermore, it highlights the innovative roles of TLR10 and miR-29a-3p in improving transplantation outcomes. An in-depth understanding of the molecular mechanisms underlying the host immune response after decellularized matrix transplantation provides new directions for the repair of tissue defects.

Keywords

Acknowledgement

This study was supported by grants from the National Natural Science Foundation of China (12272251, 12002232, 31870934) and the General Program for Basic Research of Shanxi Province (202103021223100).

References

  1. Akbarpour, M., Wu, Q., Liu, X. P., Sun, H. Y., Lecuona, E., Tomic, R., Bhorade, S., Mohanakumar, T. and Bharat, A. (2019) Clinical relevance of lung-restricted antibodies in lung transplantation. Hum. Immunol. 80, 595-601.
  2. Alaby Pinheiro Faccioli, L., Suhett Dias, G., Hoff, V., Lemos Dias, M., Ferreira Pimentel, C., Hochman-Mendez, C., Braz Parente, D., Labrunie, E., Souza Mourao, P. A., Rogerio de Oliveira Salvalaggio, P., Goldberg, A. C., Campos de Carvalho, A. C. and Dos Santos Goldenberg, R. C. (2022) Optimizing the decellularized porcine liver scaffold protocol. Cells Tissues Organs 211, 385-394.
  3. Antmen, E., Vrana, N. E. and Hasirci, V. (2021) The role of biomaterials and scaffolds in immune responses in regenerative medicine: macrophage phenotype modulation by biomaterial properties and scaffold architectures. Biomater. Sci. 9, 8090-8110.
  4. Asberg, A. E. and Videm, V. (2005) Activation of neutrophil granulocytes in an in vitro model of a cardiopulmonary bypass. Artif. Organs 29, 927-936.
  5. Barone, A. A. L., Mastroianni, M., Farkash, E. A., Mallard, C., Albritton, A., Torabi, R., Leonard, D. A., Kurtz, J. M., Sachs, D. H. and Cetrulo, C. L., Jr. (2015) Genetically modified porcine split-thickness skin grafts as an alternative to allograft for provision of temporary wound coverage: preliminary characterization. Burns 41, 565-574.
  6. Bernardini, R., Varvaras, D., D'Amico, F., Bielli, A., Scioli, M. G., Coniglione, F., Rossi, P., Buonomo, O. C., Petrella, G., Mattei, M. and Orlandi, A. (2020) Biological acellular pericardial mesh regulated tissue integration and remodeling in a rat model of breast prosthetic implantation. J. Biomed. Mater. Res. Part B 108, 577-590.
  7. Biguetti, C. C., Silveira, E. V., Araujo-Pires, A. C., Trombone, A. P. F., Letra, A., Silva, R. M. and Garlet, G. (2016) DAMPS/MYD88 axis in the modulation of host inflammatory and healing responses to classic titanium-based biomaterials in vivo. Cytokine 87, 144.
  8. Bilodeau, C., Goltsis, O., Rogers, I. M. and Post, M. (2020) Limitations of recellularized biological scaffolds for human transplantation. J. Tissue Eng. Regen. Med. 14, 521-538.
  9. Bing, Z., Feng, L., Wu, C.-S., Du, J.-T., Liu, Y.-F. and Liu, S.-X. (2019) Acellular dermal matrix contributes to epithelialization in patients with chronic sinusitis. J. Biomater. Appl. 33, 1053-1059.
  10. Broyles, J. M., Liao, E. C., Kim, J., Heistein, J., Sisco, M., Karp, N., Lau, F. H. and Chun, Y. S. (2021) Acellular dermal matrix-associated complications in implant-based breast reconstruction: a multicenter, prospective, randomized controlled clinical trial comparing two human tissues. Plast. Reconstr. Surg. 148, 493-500.
  11. Bruyneel, A. A. N. and Carr, C. A. (2017) Ambiguity in the presentation of decellularized tissue composition: the need for standardized approaches. Artif. Organs 41, 778-784.
  12. Byun, I. H., Kim, C. W. and Park, T. H. (2019) The modified keystone flap for pressure ulcers a modification of the keystone flap with rotation and advancement. Ann. Plast. Surg. 82, 299-303.
  13. Carnel, N., Lancia, H. H., Guinier, C. and Benichou, G. (2023) Pathways of antigen recognition by T cells in allograft rejection. Transplantation 107, 827-837.
  14. Chang, C.-T. (2023) The hemostatic effect and wound healing of novel collagen-containing polyester dressing. J. Biomater. Sci. Polym. Ed. 34, 2124-2143.
  15. Chen, L., Yang, J., Wang, D. Y., Jiang, J. M., Zhang, B. D., Zhao, Z. J., Chen, X. L. and Lv, D. L. (2024) Multicenter effect analysis of one-step acellular dermis combined with autologous ultra-thin split thickness skin composite transplantation in treating burn and traumatic wounds. Int. Wound J. 21, e14341.
  16. Chen, M. S., Jin, Y., Han, X., Wang, N., Deng, X. Y. and Liu, H. P. (2017) MSCs on an acellular dermal matrix (ADM) sourced from neonatal mouse skin regulate collagen reconstruction of granulation tissue during adult cutaneous wound healing. RSC Adv. 7, 22998-23010.
  17. Croes, M., Kruyt, M. C., Boot, W., Pouran, B., Braham, M. V. J., Pakpahan, S. A., Weinans, H., Vogely, H. C., Fluit, A. C., Dhert, W. J. A., Alblas, J. and Oner, F. C. (2019) The role of bacterial stimuli in inflammation-driven bone formation. Eur. Cells Mater. 37, 402-419.
  18. Da, L. C., Huang, Y. Z., Xie, H. Q., Zheng, B. H., Huang, Y. C. and Du, S. R. (2021) Membranous extracellular matrix-based scaffolds for skin wound healing. Pharmaceutics 13, 1796.
  19. Dabare, P. R. L., Bachhuka, A., Palms, D., Parkinson-Lawrence, E., Hayball, J., Mierczynska, A. and Vasilev, K. (2022) Surface chemistry mediated albumin adsorption, conformational changes and influence on innate immune responses. Appl. Surf. Sci. 596, 153518.
  20. Dabare, P. R. L., Bachhuka, A., Parkinson-Lawrence, E. and Vasilev, K. (2021) Surface nanotopography mediated albumin adsorption, unfolding and modulation of early innate immune responses. Mater. Today Adv. 12, 100187.
  21. Dalgaard, L. T., Sorensen, A. E., Hardikar, A. A. and Joglekar, M. V. (2022) The microRNA-29 family: role in metabolism and metabolic disease. Am. J. Physiol. Cell Physiol. 323, C367-C377.
  22. Daly, K. A., Liu, S., Agrawal, V., Brown, B. N., Huber, A., Johnson, S. A., Reing, J., Sicari, B., Wolf, M., Zhang, X. and Badylak, S. F. (2012) The host response to endotoxin-contaminated dermal matrix. Tissue Eng. Part A 18, 1293-1303.
  23. Das, P., Mishra, R., Devi, B., Rajesh, K., Basak, P., Roy, M., Roy, P., Lahiri, D. and Nandi, S. K. (2021) Decellularized xenogenic cartilage extracellular matrix (ECM) scaffolds for the reconstruction of osteochondral defects in rabbits. J. Mater. Chem. B 9, 4873-4894.
  24. de Almeida Coelho, Z. B., Mourao, L. C., Medeiros Rodrigues, B. C., Cardoso-Oliveira, G. P., Hincapie, R., Sanhueza-Chavez, C., Finn, M. G., Fernandes Fontes, C. J., Marques, A. F. and Braga, E. M. (2019) Preliminary assessment of anti-α-Gal IgG and IgM levels in patients with patent plasmodium vivax infection. Mem. Inst. Oswaldo Cruz 114, 190145.
  25. de Paula, A. G. P., de Lima, J. D., Bastos, T. S. B., Czaikovski, A. P., Dos Santos Luz, R. B., Yuasa, B. S., Smanioto, C. C. S., Robert, A. W. and Braga, T. T. (2023) Decellularized extracellular matrix: the role of this complex biomaterial in regeneration. Acs OMEGA 8, 22256-22267.
  26. De Trez, C., Khan, S. and Magez, S. (2020) T. brucei infections abrogate diverse plasma cell-mediated effector B cell responses, independently of their specificity, affinity and host genetic background. PLoS Negl. Trop. Dis. 14, e0008358.
  27. DePamphilis, M. A., Cauley, R. P., Sadeq, F., Lydon, M., Sheridan, R. L., Winograd, J. M. and Driscoll, D. N. (2022) Reconstruction of the upper extremity high-voltage electrical injury: a pediatric burn hospital's 13-year experience. J. Burn Care Res. 43, 696-703.
  28. Di, H., Xia, T. Y., Zhang, M., Guo, H., Cao, D., Xie, J. and Xia, C. (2022) Reconstruction of giant defects due to electrical and radiation burns in the lower leg with free anterolateral thigh flaps. J. Plast. Reconstr. Aes. 75, 1596-1601.
  29. Ding, Z., Dan, N. H. and Chen, Y. N. (2022) Study of a hydrophilic healing-promoting porcine acellular dermal matrix. Processes 10, 916.
  30. Duan, T. H., Du, Y., Xing, C. S., Wang, H. Y. Y. and Wang, R. F. (2022) Toll-like receptor signaling and its role in cell-mediated immunity. Front. Immunol. 13, 812774.
  31. Duisit, J., Orlando, G., Debluts, D., Maistriaux, L., Xhema, D., de Bisthoven, Y.-A. J., Galli, C., Peloso, A., Behets, C., Lengele, B. and Gianello, P. (2018) Decellularization of the porcine ear generates a biocompatible, nonimmunogenic extracellular matrix platform for face subunit bioengineering. Ann. Surg. 267, 1191-1201.
  32. Evren, S., Loai, Y., Antoon, R., Islam, S., Yeger, H., Moore, K., Wong, K., Gorczynski, R. and Farhat, W. A. (2010) Urinary bladder tissue engineering using natural scaffolds in a porcine model: role of toll-like receptors and impact of biomimetic molecules. Cells Tissues Organs 192, 250-261.
  33. Fernandez-Moure, J. S., Van Eps, J. L., Scherba, J. C., Yazdi, I. K., Robbins, A., Cabrera, F., Vatsaas, C. J., Moreno, M., Weiner, B. K. and Tasciotti, E. (2021) Addition of platelet-rich plasma supports immune modulation and improved mechanical integrity in alloderm mesh for ventral hernia repair in a rat model. J. Tissue Eng. Regen. Med. 15, 3-13.
  34. Fitzgerald, K. A. and Kagan, J. C. (2020) Toll-like receptors and the control of immunity. Cell 180, 1044-1066.
  35. Franz, S., Rammelt, S., Scharnweber, D. and Simon, J. C. (2011) Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32, 6692-6709.
  36. Frischauf, N., Strasser, U. and Preiner, J. (2021) Effects of Immunoglobulin G subclass on the classical complement activation. Eur. Biophys. J. Biophys. Lett. 50, 97.
  37. Gock, H., Salvaris, E., Murray-Segal, L., Mottram, P., Han, W., Pearse, M. J., Goodman, D. J., Cowan, P. J. and d'Apice, A. J. (2000) Hyperacute rejection of vascularized heart transplants in BALB/c Gal knockout mice. Xenotransplantation 7, 237-246.
  38. Gorbet, M. B. and Sefton, M. V. (2004) Biomaterial-associated thrombosis: roles of coagulation factors, complement, platelets and leukocytes. Biomaterials 25, 5681-5703.
  39. Guan, L.-F., Fang, C., Wang, X.-N., Luo, Q.-Y. and Wu, Y.-S. (2021) An exploration of the method for repairing knee joint trauma-induced skin defects with a saphenous flap. J. Biomater. Tissue Eng. 11, 1848-1852.
  40. Hakansson, K. E. J., Sollie, O., Simons, K. H., Quax, P. H. A., Jensen, J. and Nossent, A. Y. (2018) Circulating small non-coding RNAs as biomarkers for recovery after exhaustive or repetitive exercise. Front. Physiol. 9, 1136.
  41. Halm, D., Leibig, N., Martens, J., Stark, G. B., Gross, T., Zimmermann, S., Finkenzeller, G. and Lampert, F. (2021) Direct comparison of the immunogenicity of major histocompatibility complex-I and -II deficient mesenchymal stem cells in vivo. Biol. Chem. 402, 693-702.
  42. He, J., Li, Z. N., Yu, T. H., Wang, W. Z., Tao, M. H., Wang, S. L., Ma, Y. Z., Fan, J., Tian, X. H., Wang, X. H., Javed, R. and Ao, Q. (2020) In vitro and in vivo biocompatibility study on acellular sheep periosteum for guided bone regeneration. Biomed. Mater. 15, 015013.
  43. Heo, C. Y., Kang, B., Jeong, J. H., Kim, K. and Myung, Y. (2022) Acellular dermal matrix and bone cement sandwich technique for chest wall reconstruction. Arch. Plast. Surg. 49, 25-28.
  44. Hess, N. J., Jiang, S., Li, X. Y., Guan, Y. and Tapping, R. I. (2017) TLR10 is a B cell intrinsic suppressor of adaptive immune responses. J. Immunol. 198, 699-707.
  45. Hildebrandt, F., Mohammed, M., Dziedziech, A., Bhandage, A. K., Divne, A.-M., Barrenas, F., Barragan, A., Henriksson, J. and Ankarklev, J. (2023) scDual-Seq of Toxoplasma gondii-infected mouse BMDCs reveals heterogeneity and differential infection dynamics. Front. Immunol. 14, 1224591.
  46. Holton, L. H., Haerian, H., Silverman, R. P., Chung, T., Elisseeff, J. H., Goldberg, N. H. and Slezak, S. (2005) Improving long-term projection in nipple reconstruction using human acellular dermal matrix - an animal model. Ann. Plast. Surg. 55, 304-309.
  47. Hou, X., Zhang, E., Mao, Y., Luan, J. and Fu, S. (2023) A bibliometric analysis of research on decellularized matrix for two decades. Tissue Eng. Part C 29, 395-409.
  48. Hu, D., Zhang, D. Y., Liu, B., Liu, Y., Zhou, Y., Yu, Y. H., Shen, L. J., Long, C. L., Zhang, D., Liu, X., Lin, T., He, D. W., Xu, T., Timashev, P., Butnaru, D., Zhang, Y. Y. and Wei, G. H. (2020) Human ucMSCs seeded in a decellularized kidney scaffold attenuate renal fibrosis by reducing epithelial-mesenchymal transition via the TGF-beta/Smad signaling pathway. Pediatr. Res. 88, 192-201.
  49. Hu, S. X., Kuwabara, R., Chica, C. E. N., Smink, A. M., Koster, T., Medina, J. D., de Haan, B. J., Beukema, M., Lakey, J. R. T., Garcia, A. J. and de Vos, P. (2021) Toll-like receptor 2-modulating pectin-polymers in alginate-based microcapsules attenuate immune responses and support islet-xenograft survival. Biomaterials 266, 120460.
  50. Huai, G., Qi, P., Yang, H. and Wang, Y. (2016) Characteristics of α-Gal epitope, anti-Gal antibody, α1,3 galactosyltransferase and its clinical exploitation (review). Int. J. Mol. Med. 37, 11-20.
  51. Huang, C.-C. (2021) Microporous scaffolds via a designed decellularization procedure combined with papain-containing reagent treatments after supercritical fluid of carbon dioxide. Mater. Lett. 304, 130539.
  52. Huang, J. W., Xu, Y. M., Li, Z. B., Murphy, S. V., Zhao, W. X., Liu, Q. Q., Zhu, W. D., Fu, Q., Zhang, Y. P. and Song, L. J. (2016) Tissue performance of bladder following stretched electrospun silk fibroin matrix and bladder acellular matrix implantation in a rabbit model. J. Biomed. Mater. Res. Part A 104, 9-16.
  53. Huang, Q., Fang, Y., Wang, Y. and Liao, H. (2022) Clinical observation on healing of tarsal plate defect after reconstruction with xenogeneic acellular dermal matrix. BMC Ophthalmol. 22, 326.
  54. Isidan, A., Liu, S., Chen, A. M., Zhang, W., Li, P., Smith, L. J., Hara, H., Cooper, D. K. C. and Ekser, B. (2021) Comparison of porcine corneal decellularization methods and importance of preserving corneal limbus through decellularization. PLoS One 16, e0243682.
  55. Jackson, S. R. and Roman, S. (2019) Matriderm and split skin grafting for full-thickness pediatric facial burns. J. Burn Care Res. 40, 251-254.
  56. Jian, L. L., Sun, L., Li, C. H., Yu, R. H., Ma, Z. Z., Wang, X. Y., Zhao, J. X. and Liu, X. Y. (2019) Interleukin-21 enhances Toll-like receptor 2/4-mediated cytokine production via phosphorylation in the STAT3, Akt and p38 MAPK signalling pathways in human monocytic THP-1 cells. Scand. J. Immunol. 89, e12761.
  57. Jiang, X., Wang, Y., Qiu, W., Huang, C., Liu, Z., Ding, T., Shi, D. and Li, X. (2019) Corneal stromal transplantation with human-derived acellular dermal matrix for pellucid marginal corneal degeneration: a nonrandomized clinical trial. Transplantation 103, E172-E179.
  58. Jing, L., Rota, S., Olivier, F., Momier, D., Guigonis, J.-M., Schaub, S., Samson, M., Bouler, J.-M., Scimeca, J.-C., Rochet, N. and Lagadec, P. (2021) Proteomic analysis identified LBP and CD14 as key proteins in blood/biphasic calcium phosphate microparticle interactions. Acta Biomater. 127, 298-312.
  59. Kawasaki, T. and Kawai, T. (2014) Toll-like receptor signaling pathways. Front. Immunol. 5, 461.
  60. Kedar, D. J., Suh, H. S., Park, C. J. and Hong, J. P. (2024) Soft tissue reconstruction after revascularization. Int. J. Low. Extrem. Wounds 23, 27-32.
  61. Kew, R. R. (2019) The vitamin D binding protein and inflammatory injury: a mediator or sentinel of tissue damage? Front. Endocrinol. (Lausanne) 10, 470.
  62. Khoury, W. E., Fahim, R., Sciulli, J. M. and Ehredt, D. J., Jr. (2012) Management of failed and infected first metatarsophalangeal joint implant arthroplasty by reconstruction with an acellular dermal matrix: a case report. J. Foot Ankle Surg. 51, 669-674.
  63. Knapp, B. and Deane, C. M. (2016) T-cell receptor binding affects the dynamics of the peptide/MHC-I complex. J. Chem. Inf. Model. 56, 46-53.
  64. Kumar, N., Mathew, D. D., Gangwar, A. K., Remya, V., Muthalavi, M. A., Maiti, S. K. and Sharma, A. K. (2014) Reconstruction of large ventro-lateral hernia in a buffalo with acellular dermal matrix: a method for treating large hernias in animals - a case report. Vet. Arh. 84, 691-699.
  65. Lacroix, G., Jeanne, M., Martinot, V. and Pasquesoone, L. (2023) "Extensive necrosis following extravasation of alkali in the crease of the elbow after voluntary intravenous injection: a case report". Ann. Chir. Plast. 68, 81-85.
  66. Li, C., Xu, Y. M. and Li, H. B. (2013) Preliminary experimental study of urethral reconstruction with tissue engineering and RNA interference techniques. Asian J. Androl. 15, 430-433.
  67. Li, D. S., Sun, W. Q., Wang, T., Gao, Y. L., Wu, J. L., Xie, Z. P., Zhao, J. J., He, C. L., Zhu, M. F., Zhang, S. M., Wang, P. and Mo, X. M. (2021) Evaluation of a novel tilapia-skin acellular dermis matrix rationally processed for enhanced wound healing. Mater. Sci. Eng. C 127, 112202.
  68. Li, G., Shen, Q., Zhou, P., Liu, H. and Chen, J. (2023) Acellular dermal matrix for one-stage treatment of lower extremity full-thickness skin defect: a case series. BMC Surg. 23, 17.
  69. Liang, N. E., Griffin, M. F., Berry, C. E., Parker, J. B., Downer, M. A., Wan, D. C. and Longaker, M. T. (2023) Attenuating chronic fibrosis: decreasing foreign body response with acellular dermal matrix. Tissue Eng. Part B 29, 671-680.
  70. Lin, Z. K., Nica, C., Sculean, A. and Asparuhova, M. B. (2020) Enhanced wound healing potential of primary human oral fibroblasts and periodontal ligament cells cultured on four different porcine-derived collagen matrices. Materials 13, 3819.
  71. Liu, K., He, Y. and Lu, F. (2022) Research progress on the immunogenicity and regeneration of acellular adipose matrix: a mini review. Front. Bioeng. Biotechnol. 10, 881523.
  72. Liu, K. Y., He, Y. F., Yao, Y., Zhang, Y. C., Cai, Z. H., Ru, J. J., Zhang, X. D., Jin, X. X., Xu, M. M., Li, Y. B., Ma, Q. Z., Gao, J. H. and Lu, F. (2021a) Methoxy polyethylene glycol modification promotes adipogenesis by inducing the production of regulatory T cells in xenogeneic acellular adipose matrix. Mater. Today Bio 12, 100161.
  73. Liu, Z. N., Liu, X. Z., Bao, L. H., Liu, J. J., Zhu, X. Q., Mo, X. M. and Tang, R. (2021b) The evaluation of functional small intestinal submucosa for abdominal wall defect repair in a rat model: potent effect of sequential release of VEGF and TGF-beta 1 on host integration. Biomaterials 276, 120999.
  74. Love, R. J. and Jones, K. S. (2013) The recognition of biomaterials: pattern recognition of medical polymers and their adsorbed biomolecules. J. Biomed. Mater. Res. Part A 101, 2740-2752.
  75. Lucke, S., Hoene, A., Walschus, U., Kob, A., Pissarek, J. W. and Schlosser, M. (2015) Acute and chronic local inflammatory reaction after implantation of different extracellular porcine dermis collagen matrices in rats. BioMed Res. Int. 2015, 938059.
  76. Luo, H. L., Zhang, Y. J., Zhang, Z. Q. and Jin, Y. (2012) The protection of MSCs from apoptosis in nerve regeneration by TGF beta 1 through reducing inflammation and promoting VEGF-dependent angiogenesis. Biomaterials 33, 4277-4287.
  77. Marques, A., Miranda, G., Silva, F., Pinto, P. and Carvalho, O. (2021) Review on current limits and potentialities of technologies for biomedical ceramic scaffolds production. J. Biomed. Mater. Res. Part B 109, 377-393.
  78. Martin, K. E. and Garcia, A. J. (2021) Macrophage phenotypes in tissue repair and the foreign body response: implications for biomaterial-based regenerative medicine strategies. Acta Biomater. 133, 4-16.
  79. Masoomikarimi, M. and Salehi, M. (2022) Modulation of the immune system promotes tissue regeneration. Mol. Biotechnol. 64, 599-610.
  80. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S. and Janeway, C. A., Jr. (1998) MyD88 is an adaptor protein in the Toll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253-258.
  81. Melandri, D., Marongiu, F., Carboni, A., Rubino, C., Razzano, S., Purpura, V., Minghetti, P. and Bondioli, E. (2020) A new human-derived acellular dermal matrix for 1-stage coverage of exposed tendons in the foot. Int. J. Low. Extrem. Wounds 19, 78-85.
  82. Melkonyan, K. I., Popandopulo, K. I., Bazlov, S. B., Verevkin, A. A., Rusinova, T. V., Asyakina, A. S., Suprun, I. V., Zaborova, V. A. and Gurevich, K. G. (2023) Results of experimental hernioplasty with acellular dermal matrix. Bull. Exp. Biol. Med. 174, 514-517.
  83. Mesina, M., Mindrila, I., Mesina-Botoran, M. I., Mindrila, L. A., Farhangee, A. and Pirici, I. (2023) Optimization techniques of single-detergent based protocols for heart tissue decellularization. Curr. Health Sci. J. 49, 156-162.
  84. Mishra, V. and Pathak, C. (2019) Human Toll-Like Receptor 4 (hTLR4): structural and functional dynamics in cancer. Int. J. Biol. Macromol. 122, 425-451.
  85. Moffat, D., Ye, K. and Jin, S. (2022) Decellularization for the retention of tissue niches. J. Tissue Eng. 13, 20417314221101151.
  86. Morris, A. H., Stamer, D. K. and Kyriakides, T. R. (2017) The host response to naturally-derived extracellular matrix biomaterials. Semin. Immunol. 29, 72-91.
  87. Moulod, M. and Moghaddam, S. (2022) Insights from molecular dynamics simulations of albumin adsorption on hydrophilic and hydrophobic surfaces. J. Mol. Graph. Model. 112, 108120.
  88. Nafar, M., Kalantari, S., Samavat, S., Omrani, M. D., Arsang-Jang, S., Taheri, M. and Ghafouri-Fard, S. (2020) Downregulation of protein inhibitor of activated STAT (PIAS) 1 is possibly involved in the process of allograft rejection. Transplant. Proc. 52, 414-418.
  89. Nahabedian, M. Y., Kabaria, N., Lombardi, J., Leung, B. K. and Sandor, M. (2023) Betadine soaking of silicone coupons minimally impacts acellular dermal matrix incorporation in a preclinical primate model. Plast. Reconstr. Surg. 152, 1262-1272.
  90. Nayakawde, N. B., Methe, K., Banerjee, D., Berg, M., Premaratne, G. U. and Olausson, M. (2020) In vitro regeneration of decellularized pig esophagus using human amniotic stem cells. BioRes. Open Access 9, 22-36.
  91. Obermann, H.-L., Eberhardt, I., Yu, P., Kaufmann, A. and Bauer, S. (2019) RNA-DNA hybrids and ssDNA differ in intracellular half-life and toll-like receptor 9 activation. Immunobiology 224, 843-851.
  92. Oskam, N., Damelang, T., Streutker, M., Heer, P., Nouta, J., Koeleman, C., Van Coillie, J., Wuhrer, M., Vidarsson, G. and Rispens, T. (2023) Factors affecting IgG4-mediated complement activation. Front. Immunol. 14, 1087532.
  93. Park, J. H., Wee, S. Y. and Kim, Y. H. (2022) The utility of novel fish-skin derived acellular dermal matrix (kerecis) as a wound dressing material. Wound Repair Regen. 30, A55-A56.
  94. Platz, J., Bonenfant, N. R., Uhl, F. E., Coffey, A. L., McKnight, T., Parsons, C., Sokocevic, D., Borg, Z. D., Lam, Y.-W., Deng, B., Fields, J. G., DeSarno, M., Loi, R., Hoffman, A. M., Bianchi, J., Dacken, B., Petersen, T., Wagner, D. E. and Weiss, D. J. (2016) Comparative decellularization and recellularization of wild-type and alpha 1,3 galactosyltransferase knockout pig lungs: a model for ex vivo xenogeneic lung bioengineering and transplantation. Tissue Eng. Part C 22, 725-739.
  95. Plymale, M. A., Davenport, D. L., Walsh-Blackmore, S., Hess, J., Griffiths, W. S., Plymale, M. C., Totten, C. F. and Roth, J. S. (2020) Costs and complications associated with infected mesh for ventral hernia repair. Surg. Infect. (Larchmt.) 21, 344-349.
  96. Radwan, J., Babik, W., Kaufman, J., Lenz, T. L. and Winternitz, J. (2020) Advances in the evolutionary understanding of MHC polymorphism. Trends Genet. 36, 298-311.
  97. Rafikova, G., Piatnitskaia, S., Shapovalova, E., Chugunov, S., Kireev, V., Ialiukhova, D., Bilyalov, A., Pavlov, V. and Kzhyshkowska, J. (2023) Interaction of ceramic implant materials with immune system. Int. J. Mol. Sci. 24, 4200.
  98. Sadowska, J. M. and Ginebra, M.-P. (2020) Inflammation and biomaterials: role of the immune response in bone regeneration by inorganic scaffolds. J. Mater. Chem. B 8, 9404-9427.
  99. Salinas, F., Robla, D., Meana, A., Pevida, M., Martinez Magide, G., Sanchez Nuno, C., Martin Suarez, L., Astudillo Gonzalez, A., Garcia, E. and Junquera, L. (2022) Novel technique of development of human derived acellular dermal matrix. Cell Tissue Banking 23, 385-394.
  100. Salinas Ramila, F., Robla Costales, D., Junquera Gutierrez, L. M., Pevida Lopez, M., Llames, S., Martinez Magide, G., Sanchez Nuno, C. and Martin Suarez, L. (2021) Development of human derived acellular dermal matrix: novel technique in pandemic times. Br. J. Surg. 108, iii3.
  101. Saricilar, E. C. and Huang, S. (2021) Comparison of porcine and human acellular dermal matrix outcomes in wound healing: a deep dive into the evidence. Arch. Plast. Surg. 48, 433-439.
  102. Shafeghat, M., Kazemian, S., Aminorroaya, A., Aryan, Z. and Rezaei, N. (2022) Toll-like receptor 7 regulates cardiovascular diseases. Int. Immunopharmacol. 113, 109390.
  103. Shao, S., Sun, X., Chen, Y., Zhan, B. and Zhu, X. (2019) Complement evasion: an effective strategy that parasites utilize to survive in the host. Front. Microbiol. 10, 532.
  104. Shen, H., Song, Y., Colangelo, C. M., Wu, T., Bruce, C., Scabia, G., Galan, A., Maffei, M. and Goldstein, D. R. (2012) Haptoglobin activates innate immunity to enhance acute transplant rejection in mice. J. Clin. Invest. 122, 383-387.
  105. Shepherd, F. R. and McLaren, J. E. (2020) T cell immunity to bacterial pathogens: mechanisms of immune control and bacterial evasion. Int. J. Mol. Sci. 21, 6144.
  106. Shin, Y. H., Park, S. Y. and Kim, J. K. (2019) Comparison of systematically combined detergent and nuclease-based decellularization methods for acellular nerve graft: an ex vivo characterization and in vivo evaluation. J. Tissue Eng. Regen. Med. 13, 1241-1252.
  107. Shirani, A., Ganji, F., Golmohammadi, M., Hashemi, S. M., Mozafari, M., Amoabediny, G., Osguei, N. K. and Samadikuchaksaraei, A. (2021) Cross-linked acellular lung for application in tissue engineering: effects on biocompatibility, mechanical properties and immunological responses. Mater. Sci. Eng. C 122, 111938.
  108. Talaei-Khozani, T. and Yaghoubi, A. (2022) An overview of post transplantation events of decellularized scaffolds. Transpl. Immunol. 74, 101640.
  109. Tardalkar, K., Marsale, T., Bhamare, N., Kshersagar, J., Chaudhari, L. and Joshi, M. G. (2022) Heparin immobilization of tissue engineered xenogeneic small diameter arterial scaffold improve endothelialization. Tissue Eng. Regener. Med. 19, 505-523.
  110. Tellarini, A., Garutti, L., Corno, M., Tamborini, F., Paganini, F., Fasoli, V., Di Giovanna, D. and Valdatta, L. (2023) Immediate post-mastectomy prepectoral breast reconstruction with animal derived acellular dermal matrices: a systematic review. J. Plast. Reconstr. Aesthet. Surg. 86, 94-108.
  111. Ueha, S., Shand, F. H. W. and Matsushima, K. (2012) Cellular and molecular mechanisms of chronic inflammation-associated organ fibrosis. Front. Immunol. 3, 71.
  112. Valdes-Lopez, J. F., Fernandez, G. J. and Urcuqui-Inchima, S. (2022) Synergistic effects of Toll-like receptor 1/2 and Toll-like receptor 3 signaling triggering interleukin 27 gene expression in chikungunya virus-infected macrophages. Front. Cell Dev. Biol. 10, 812110.
  113. Van Eps, J. L., Boada, C., Scherba, J. C., Zavlin, D., Arrighetti, N., Shi, A. R., Wang, X., Tasciotti, E., Buell, J. F., Ellsworth, W. A., Bonville, D. J. and Fernandez-Moure, J. S. (2021) Amniotic fluid allograft enhances the host response to ventral hernia repair using acellular dermal matrix. J. Tissue Eng. Regen. Med. 15, 1092-1104.
  114. Vasanthan, V., Shim, H. B., Teng, G. Q., Belke, D., Svystonyuk, D., Deniset, J. F. and Fedak, P. W. M. (2023) Acellular biomaterial modulates myocardial inflammation and promotes endogenous mechanisms of postinfarct cardiac repair. J. Thorac. Cardiovasc. Surg. 165, e122-e140.
  115. Wade, C., Wolf, S. E., Salinas, R., Jones, J. A., Rivera, R., Hourigan, L., Baskin, T., Linfoot, J., Mann, E. A., Chung, K. and Dubick, M. (2010) Loss of protein, immunoglobulins, and electrolytes in exudates from negative pressure wound therapy. Nutr. Clin. Pract. 25, 510-516.
  116. Wang, H. D. and Sun, W. Q. (2023) Comparative proteomic analysis of regenerative acellular matrices: the effects of tissue source and processing method. J. Biomed. Mater. Res. Part B 111, 2002-2012.
  117. Wang, L. J., Liu, L. P., Gu, X. L., Wang, M. and Liu, L. M. (2018) Implantation of adipose-derived stem cells cures the optic nerve injury on rats through inhibiting the expression of inflammation factors in the TLR4 signaling pathway. Eur. Rev. Med. Pharmacol. Sci. 22, 1196-1202.
  118. Wang, Y., Xu, Y., Zhou, G., Liu, Y. and Cao, Y. (2021) Biological evaluation of acellular cartilaginous and dermal matrixes as tissue engineering scaffolds for cartilage regeneration. Front. Cell Dev. Biol. 8, 624337.
  119. Wang, Z., Guo, Y., Zhang, Y., Wu, L., Wang, L., Lin, Q. and Wan, B. (2023) An intriguing structural modification in neutrophil migration across blood vessels to inflammatory sites: progress in the core mechanisms. Cell Biochem. Biophys. 82, 67-75.
  120. Wei, F., Liu, S., Chen, M., Tian, G., Zha, K., Yang, Z., Jiang, S., Li, M., Sui, X., Chen, Z. and Guo, Q. (2021) Host response to biomaterials for cartilage tissue engineering: key to remodeling. Front. Bioeng. Biotechnol. 9, 664592.
  121. Wei, J., Xu, Z. H. and Yan, X. (2022) The role of the macrophage-to-myofibroblast transition in renal fibrosis. Front. Immunol. 13, 934337.
  122. Wei, Z., Zhang, J., Guo, Z., Wu, Z., Sun, Y., Wang, K. and Duan, R. (2023) Study on the preparation and properties of acellular matrix from the skin of silver carp (Hypophthalmichthys molitrix). J. Biomed. Mater. Res. Part B 111, 1328-1335.
  123. Witherel, C. E., Graney, P. L., Freytes, D. O., Weingarten, M. S. and Spiller, K. L. (2016) Response of human macrophages to wound matrices in vitro. Wound Repair Regen. 24, 514-524.
  124. Witte, M. B. and Barbul, A. (1997) General principles of wound healing. Surg. Clin. North Am. 77, 509-528.
  125. Wong, M. L., Wong, J. L., Athanasiou, K. A. and Griffiths, L. G. (2013) Stepwise solubilization-based antigen removal for xenogeneic scaffold generation in tissue engineering. Acta Biomater. 9, 6492-6501.
  126. Woo, S. J., Ha, J. H. and Jin, U. S. (2021) Comparison of irradiated and non-irradiated acellular dermal matrices in breast reconstruction under radiotherapy. Arch. Plast. Surg. 48, 33-43.
  127. Wu, X., Wang, C. Y., Hao, P. F., He, F., Yao, Z. H. and Zhang, X. W. (2021) Adsorption properties of albumin and fibrinogen on hydrophilic/hydrophobic TiO2 surfaces: a molecular dynamics study. Colloids Surf. B 207, 111994.
  128. Wu, Z., Zhou, Y., Li, N., Huang, M., Duan, H., Ge, J., Xiang, P. and Wang, Z. (2009) The use of phospholipase A2 to prepare acellular porcine corneal stroma as a tissue engineering scaffold. Biomaterials 30, 3513-3522.
  129. Xia, W., Lin, C., Tu, Z., Li, Y. and Shen, G. (2023) Preparation of laser microporous porcine acellular dermal matrix and observation of wound transplantation. Cell Tissue Banking 24, 191-202.
  130. Xu, H., Sandor, M., Qi, S., Lombardi, J., Connor, J., McQuillan, D. J. and Iannotti, J. P. (2012) Implantation of a porcine acellular dermal graft in a primate model of rotator cuff repair. J. Shoulder Elbow Surg. 21, 580-588.
  131. Xu, M., Su, T., Jin, X., Li, Y., Yao, Y., Liu, K., Chen, K., Lu, F. and He, Y. (2022) Inflammation-mediated matrix remodeling of extracellular matrix-mimicking biomaterials in tissue engineering and regenerative medicine. Acta Biomater. 151, 106-117.
  132. Yamanaka, H., Morimoto, N. and Yamaoka, T. (2020) Decellularization of submillimeter-diameter vascular scaffolds using peracetic acid. J. Artif. Organs 23, 156-162.
  133. Yang, J., Xu, Y., Luo, S., Dang, H. and Cao, M. (2022) Effect of cryoprotectants on rat kidney decellularization by freeze-thaw process. Cryobiology 105, 71-82.
  134. Yang, Z., Li, H., Tian, Y., Fu, L. W., Gao, C. J., Zhao, T. Y., Cao, F. Y., Liao, Z. Y., Yuan, Z. G., Liu, S. Y. and Guo, Q. Y. (2021) Biofunctionalized structure and ingredient mimicking scaffolds achieving recruitment and chondrogenesis for staged cartilage regeneration. Front. Cell Dev. Biol. 9, 655440.
  135. Yao, Z. X., Li, J. H., Xiong, H., Cui, H. M., Ning, J. X., Wang, S. K., Ouyang, X. Y., Qian, Y. and Fan, C. Y. (2021) MicroRNA engineered umbilical cord stem cell-derived exosomes direct tendon regeneration by mTOR signaling. J. Nanobiotechnol. 19, 169.
  136. Ye, C., Chen, J., Qu, Y., Qi, H., Wang, Q. F., Yang, Z., Wu, A. M., Wang, F. X. and Li, P. Y. (2022) Naringin in the repair of knee cartilage injury via the TGF-beta/ALK/Smad2/3 signal transduction pathway combined with an acellular dermal matrix. J. Orthop. Transl. 32, 1-11.
  137. Yoo, B. W., Kong, Y. T., Chae, S. W., Kim, K. N., Song, B. and Kim, J. (2023) Comparison of the characteristics of three acellular dermal matrices subjected to distinct processing methods using five types of histochemical staining. Aesthetic Plast. Surg. 47, 1315-1323.
  138. Zajonc, D. M. (2020) Unconventional peptide presentation by classical MHC class I and implications for T and NK cell activation. Int. J. Mol. Sci. 21, 7561.
  139. Zemmyo, D., Yamamoto, M., Miyata, S. (2020) Fundamental study of decellularization method using cyclic application of high hydrostatic pressure. Micromachines 11, 1008.
  140. Zhang, F. Y., Qi, H. N., Mo, W. T., Ni, Y. Q., Zhao, Q., Wang, Y. L., Jiang, S. T., Tang, Q. C., Cheng, Y. H., Xiao, X. H. and Zhang, Y. F. (2022) Low surface accessible area nanocoral tio2 for the reduction of foreign body reaction during implantation. Adv. Healthcare Mater. 11, e2200382.
  141. Zhang, L. D., Casey, B., Galanakis, D. K., Marmorat, C., Skoog, S., Vorvolakos, K., Simon, M. and Rafailovich, M. H. (2017) The influence of surface chemistry on adsorbed fibrinogen conformation, orientation, fiber formation and platelet adhesion. Acta Biomater. 54, 164-174.
  142. Zhao, Q., Zhao, Z., Zhang, J., Ni, Y., Ouyang, S., Qi, H., Yu, Y., Miron, R. J., Tang, H. and Zhang, Y. (2023) Fn-HMGB1 adsorption behavior initiates early immune recognition and subsequent osteoinduction of biomaterials. Adv. Healthcare Mater. 13, e2301808.
  143. Zheng, X., Chen, Y. N., Dan, N. H., Dan, W. H. and Li, Z. J. (2021) Highly stable collagen scaffolds crosslinked with an epoxidized natural polysaccharide for wound healing. Int. J. Biol. Macromol. 182, 1994-2002.
  144. Zhou, R., Ren, S. Y., Li, C. F., Zhang, X. T. and Zhang, W. T. (2020a) miR-29a is a potential protective factor for fibrogenesis in gluteal muscle contracture. Physiol. Res. 69, 467-479.
  145. Zhou, Z., Kim, J. W., Qi, J., Eo, S. K., Lim, C. W. and Kim, B. (2020b) Toll-like receptor 5 signaling ameliorates liver fibrosis by inducing interferon beta-modulated IL-1 receptor antagonist in mice. Am. J. Pathol. 190, 614-629.
  146. Zuo, Y. H. and Lu, S. L. (2017) Dermis, acellular dermal matrix, and fibroblasts from different layers of pig skin exhibit different profibrotic characteristics: evidence from in vivo study. Oncotarget 8, 23613-23627.