Research Progress of Biological 3D Printing Strategy in Three-Dimensional Tissue Constructionof Functionalized Skeletal Muscle
Zhang Feihu1, Li Ting2,3,4, Lin Zhiwei1, Li Yanbing2,3,4, Huang Wenhua1,2,3,4*
1(Department of Basic Medical Sciences/Department of Human Anatomy and Tissue Embryology, Guangdong Medical University, Dongguan 523808, Guangdong,China) 2(State Key Discipline of Human Anatomy, School of Basic Medical Sciences, Southern Medical University, Guangzhou 510515,China) 3(Guangdong Provincial Key Laboratory of Medical Biomechanics, Guangzhou 510515, China) 4(Guangdong Medical 3D Printing Application Translational Engineering Technology Research Center, Guangzhou 510515, China)
Abstract:Skeletal muscle is essential for body movement, and loss of motor function due to volumetric muscle loss (VML) can limit the ability to move. Transplant surgery is the main clinical approach, however, is still limited by the morbidity of the donor site, the lack of donor tissue, and the need for a highly skilled surgical team. Biological 3D printing technology provides a more efficient and accurate method for the manufacture of functional muscles, and a feasible method for the regeneration and repair of VML muscles. This paper reviewed the research status of biological 3D printing technology in the construction of functional skeletal muscle tissue structure, as well as research progress of biological 3D printing and biological ink in functional muscle structures, mainly focusing on the construction of vascularized and neuralized skeletal muscle biomimetic tissue. The effects of various functional skeletal muscle structures constructed by 3D printing on the repair of skeletal muscle defects were summarized. Finally, development trends and existing limitations in the field were proposed.
张飞虎, 李婷, 林智伟, 李严兵, 黄文华. 生物3D打印技术用于功能性骨骼肌3D组织构建的研究进展[J]. 中国生物医学工程学报, 2024, 43(5): 620-630.
Zhang Feihu, Li Ting, Lin Zhiwei, Li Yanbing, Huang Wenhua. Research Progress of Biological 3D Printing Strategy in Three-Dimensional Tissue Constructionof Functionalized Skeletal Muscle. Chinese Journal of Biomedical Engineering, 2024, 43(5): 620-630.
[1] Shaber EP. Skeletal muscle: anatomy, physiology, and pathophysiology[J]. Dent Clin North Am, 1983,27(3):435-443. [2] Garg K, Ward CL, Hurtgen BJ, et al. Volumetric muscle loss: persistent functional deficits beyond frank loss of tissue[J]. J Orthop Res, 2015,33(1):40-46. [3] Liu J, Saul D, Boker KO, et al. Current methods for skeletal muscle tissue repair and regeneration[J]. Biomed Res Int,2018:1984879. [4] Qazi TH, Mooney DJ, Pumberger M, et al. Biomaterials based strategies for skeletal muscle tissue engineering: existing technologies and future trends[J]. Biomaterials, 2015,53:502-521. [5] Gilbert-Honick J, Grayson W. Vascularized and innervated skeletal muscle tissue engineering[J]. Adv Healthc Mater, 2020,9(1):e1900626. [6] Ostrovidov S, Salehi S, Costantini M, et al. 3D bioprinting in skeletal muscle tissue engineering[J]. Small, 2019,15(24):e1805530. [7] Fitzpatrick V, Martin-Moldes Z, Deck A, et al. Functionalized 3D-printed silk-hydroxyapatite scaffolds for enhanced bone regeneration with innervation and vascularization[J]. Biomaterials, 2021,276:120995. [8] Taymour R, Chicaiza-Cabezas NA, Gelinsky M, et al. Core-shell bioprinting of vascularizedin vitroliver sinusoid models[J]. Biofabrication, 2022,14(4):045019. [9] Zhang YS, Arneri A, Bersini S, et al. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip[J]. Biomaterials, 2016,110:45-59. [10] Bersini S, Francescato R, Moretti M. Biofabrication of 3D human muscle model with vascularization and endomysium[J]. Methods Mol Biol, 2022,2373:213-230. [11] Murphy SV, Atala A. 3D bioprinting of tissues and organs[J]. Nat Biotechnol, 2014,32(8):773-785. [12] Matai I, Kaur G, Seyedsalehi A, et al. Progress in 3D bioprinting technology for tissue/organ regenerative engineering[J]. Biomaterials, 2020,226:119536. [13] Jin Y, Shahriari D, Jeon EJ, et al. Functional skeletal muscle regeneration with thermally drawn porous fibers and reprogrammed muscle progenitors for volumetric muscle injury[J]. Adv Mater, 2021,33(14):e2007946. [14] Samandari M, Quint J, Rodriguez-delaRosa A, et al. Bioinks and bioprinting strategies for skeletal muscle tissue engineering[J]. Adv Mater, 2022,34(12):e2105883. [15] Sweeney HL, Hammers DW. Muscle contraction[J]. Cold Spring Harb Perspect Biol, 2018,10(2):a023200. [16] Laschke MW, Harder Y, Amon M, et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes[J]. Tissue Eng, 2006,12(8):2093-2104. [17] Slater CR. The structure of human neuromuscular junctions: some unanswered molecular questions[J]. Int J Mol Sci, 2017,18(10):2183. [18] Calderon JC, Bolanos P, Caputo C. The excitation-contraction coupling mechanism in skeletal muscle[J]. Biophys Rev, 2014,6(1):133-160. [19] Yue K, Trujillo-de SG, Alvarez MM, et al. Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels[J]. Biomaterials, 2015,73:254-271. [20] Hwangbo H, Lee H, Jin EJ, et al. Bio-printing of aligned GelMa-based cell-laden structure for muscle tissue regeneration[J]. Bioact Mater, 2022,8:57-70. [21] Sonaye SY, Ertugral EG, Kothapalli CR, et al. Extrusion 3D (Bio)printing of Alginate-Gelatin-Based composite scaffolds for skeletal muscle tissue engineering[J]. Materials (Basel), 2022,15(22):7945. [22] Ahmed TA, Dare EV, Hincke M. Fibrin: a versatile scaffold for tissue engineering applications[J]. Tissue Eng Part B Rev, 2008,14(2):199-215. [23] Li T, Hou J, Wang L, et al. Bioprinted anisotropic scaffolds with fast stress relaxation bioink for engineering 3D skeletal muscle and repairing volumetric muscle loss[J]. Acta Biomater, 2023,156:21-36. [24] Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity[J]. Nat Biotechnol, 2016,34(3):312-319. [25] Philips C, Terrie L, Thorrez L. Decellularized skeletal muscle: a versatile biomaterial in tissue engineering and regenerative medicine[J]. Biomaterials, 2022,283:121436. [26] Kabirian F, Mozafari M. Decellularized ECM-derived bioinks: prospects for the future[J]. Methods, 2020,171:108-118. [27] Choi YJ, Kim TG, Jeong J, et al. 3D cell printing of functional skeletal muscle constructs using skeletal muscle-derived bioink[J]. Adv Healthc Mater, 2016,5(20):2636-2645. [28] Choi YJ, Jun YJ, Kim DY, et al. A 3D cell printed muscle construct with tissue-derived bioink for the treatment of volumetric muscle loss[J]. Biomaterials, 2019,206:160-169. [29] Cui XL, Li J, Hartanto Y, et al. Advances in Extrusion 3D Bioprinting: A focus on multicomponent hydrogel-based bioinks[J].Advance Healthcare Materials, 2020, 9(15): e1901648. [30] Bolivar-Monsalve EJ, Ceballos-Gonzalez CF, Chavez-Madero C, et al. One-step bioprinting of multi-channel hydrogel filaments using chaotic advection: fabrication of pre-vascularized muscle-like tissues[J]. Advanced Healthcare Materials, 2022,11(24):e2200448. [31] Liu JC,Shahriar M, Xu HQ, et al. Cell-laden bioink circulation-assisted inkjet-based bioprinting to mitigate cell sedimentation and aggregation[J]. Biofabrication, 2022,14(4):045020. [32] Li X, Liu B, Pei B, et al. Inkjet bioprinting of biomaterials[J]. Chem Rev, 2020,120(19):10793-10833. [33] Dobos A, Van Hoorick J, Steiger W, et al. Thiol-gelatin-norbornene bioink for laser-based high-definition bioprinting[J]. Adv Healthc Mater, 2020,9(15):e1900752. [34] Koch L, Deiwick A, Franke A, et al. Laser bioprinting of human induced pluripotent stem cells-the effect of printing and biomaterials on cell survival, pluripotency, and differentiation[J]. Biofabrication, 2018,10(3):035005. [35] Derby B. Bioprinting: inkjet printing proteins and hybrid cell-containing materials and structures[J]. Journal of Materials Chemistry, 2008,18(47):5717-5721. [36] Leberfinger AN, Dinda S, Wu Y, et al. Bioprinting functional tissues[J]. Acta Biomater, 2019,95:32-49. [37] Potyondy T, Uquillas J A, Tebon P J, et al. Recent advances in 3D bioprinting of musculoskeletal tissues[J]. Biofabrication, 2021,13(2):022001. [38] Jana S, Levengood SK, Zhang M. Anisotropic materials for skeletal-muscle-tissue engineering[J]. Adv Mater, 2016, 28(48):10588-10612. [39] Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity[J]. Nat Biotechnol, 2016,34(3):312-319. [40] Fan T, Wang S, Jiang Z, et al. Controllable assembly of skeletal muscle-like bundles through 3D bioprinting[J]. Biofabrication, 2021,14(1):015009. [41] Kim W, Jang CH, Kim GH. A myoblast-laden collagen bioink with fully aligned Au nanowires for muscle-tissue regeneration[J]. Nano Lett, 2019,19(12):8612-8620. [42] Agostinacchio F, Mu X, Dire S, et al. In Situ 3D printing: opportunities with silk inks[J]. Trends Biotechnol, 2021,39(7):719-730. [435] Russell CS, Mostafavi A, Quint JP, et al. In situ printing of adhesive hydrogel scaffolds for the treatment of skeletal muscle injuries[J]. ACS Appl Bio Mater, 2020,3(3):1568-1579. [44] Endo Y, Samandari M, Karvar M, et al. Aerobic exercise and scaffolds with hierarchical porosity synergistically promote functional recovery post volumetric muscle loss[J]. Biomaterials, 2023,296:122058. [45] Thangadurai M, Ajith A, Budharaju H, et al. Advances in electrospinning and 3D bioprinting strategies to enhance functional regeneration of skeletal muscle tissue[J]. Biomater Adv, 2022,142:213135. [46] Colapicchioni V, Millozzi F, Parolini O, et al. Nanomedicine, a valuable tool for skeletal muscle disorders: challenges, promises, and limitations[J]. Wiley Interdiscip Rev Nanomed Nanobiotechnol, 2022,14(3):e1777. [47] Cha SH, Lee HJ, Koh WG. Study of myoblast differentiation using multi-dimensional scaffolds consisting of nano and micropatterns[J]. Biomater Res, 2017,21:1. [48] Lee H, Kim W, Lee J, et al. Effect of hierarchical scaffold consisting of aligned dECM nanofibers and poly(lactide-co-glycolide) struts on the orientation and maturation of human muscle progenitor cells[J]. ACS Appl Mater Interfaces, 2019,11(43):39449-39458. [49] Gilbert-Honick J, Grayson W. Vascularized and innervated skeletal muscle tissue engineering[J]. Adv Healthc Mater, 2020,9(1):e1900626. [50] Gilbert-Honick J, Iyer SR, Somers S M, et al. Engineering functional and histological regeneration of vascularized skeletal muscle[J]. Biomaterials, 2018,164:70-79. [51] Kostrominova TY. Skeletal muscle denervation: past, present and future[J]. Int J Mol Sci, 2022,23(14):7489. [52] Alcazar CA, Hu C, Rando TA, et al. Transplantation of insulin-like growth factor-1 laden scaffolds combined with exercise promotes neuroregeneration and angiogenesis in a preclinical muscle injury model[J]. Biomaterials Science, 2020,8(19):5376-5389. [53] Quint JP, Mostafavi A, Endo Y, et al. In vivo printing of nanoenabled scaffolds for the treatment of skeletal muscle injuries[J]. Adv Healthc Mater, 2021,10(10):e2002152. [54] Bolivar-Monsalve EJ, Ceballos-Gonzalez CF, Chavez-Madero C, et al. One-step mbioprinting of ulti-channel hydrogel filaments using chaotic advection: fabrication of pre-vascularized muscle-Like tissues[J]. Adv Healthc Mater, 2022,11(24):e2200448. [55] Yeo M, Lee H, Kim GH. Combining a micro/nano-hierarchical scaffold with cell-printing of myoblasts induces cell alignment and differentiation favorable to skeletal muscle tissue regeneration[J]. Biofabrication, 2016,8(3):35021. [56] Kim JH, Ko IK, Jeon MJ, et al. Pelvic floor muscle function recovery using biofabricated tissue constructs with neuromuscular junctions[J]. Acta Biomater, 2021,121:237-249. [57] Kim JH, Kim I, Seol YJ, et al. Neural cell integration into 3D bioprinted skeletal muscle constructs accelerates restoration of muscle function[J]. Nat Commun, 2020,11(1):1025. [58] Cvetkovic C, Rich MH, Raman R, et al. A 3D-printed platform for modular neuromuscular motor units[J]. Microsyst Nanoeng, 2017,3:17015. [59] Rose N, Estrada CB, Sonam S, et al. Bioengineering a miniaturized in vitro 3D myotube contraction monitoring chip to model muscular dystrophies[J]. Biomaterials, 2023,293:121935.