Embedding aligned nanofibrous architectures within 3D-printed polycaprolactone scaffolds for directed cellular infiltration and tissue regeneration

Zijie Meng; Xingdou Mu; Jiankang He; Juliang Zhang; Rui Ling; Dichen Li

doi:10.1088/2631-7990/acbd6c

Three-dimensional (3D) printing provides a promising way to fabricate biodegradable scaffolds with designer architectures for the regeneration of various tissues. However, the existing 3D-printed scaffolds commonly suffer from weak cell-scaffold interactions and insufficient cell organizations due to the limited resolution of the 3D-printed features. Here, composite scaffolds with mechanically-robust frameworks and aligned nanofibrous architectures are presented and hybrid manufactured by combining techniques of 3D printing, electrospinning, and unidirectional freeze-casting. It was found that the composite scaffolds provided volume-stable environments and enabled directed cellular infiltration for tissue regeneration. In particular, the nanofibrous architectures with aligned micropores served as artificial extracellular matrix materials and improved the attachment, proliferation, and infiltration of cells. The proposed scaffolds can also support the adipogenic maturation of adipose-derived stem cells (ADSCs) in vitro. Moreover, the composite scaffolds were found to guide directed tissue infiltration and promote nearby neovascularization when implanted into a subcutaneous model of rats, and the addition of ADSCs further enhanced their adipogenic potential. The presented hybrid manufacturing strategy might provide a promising way to produce additional topological cues within 3D-printed scaffolds for better tissue regeneration.

HTML

Reference (54)

Jun I, Han H S, Edwards J R and Jeon H 2018 Electrospun fibrous scaffolds for tissue engineering: viewpoints on architecture and fabrication Int. J. Mol. Sci. 19 745

Nikolova M P and Chavali M S 2019 Recent advances in biomaterials for 3D scaffolds: a review Bioact. Mater. 4 271–92

Youssef A, Hollister S J and Dalton P D 2017 Additive manufacturing of polymer melts for implantable medical devices and scaffolds Biofabrication 9 012002

Zhang X Y, Fang G, Leeflang S, Zadpoor A A and Zhou J 2019 Topological design, permeability and mechanical behavior of additively manufactured functionally graded porous metallic biomaterials Acta Biomater. 84 437–52

Meng Z J, He J K, Li J X, Su Y W and Li D C 2020 Melt-based, solvent-free additive manufacturing of biodegradable polymeric scaffolds with designer microstructures for tailored mechanical/biological properties and clinical applications Virtual Phys. Prototyp. 15 417–44

Jia L T et al 2020 Regeneration of human-ear-shaped cartilage with acellular cartilage matrix-based biomimetic scaffolds Appl. Mater. Today 20 100639

Li P X et al 2021 Chitosan hydrogel/3D-printed poly(ε-caprolactone) hybrid scaffold containing synovial mesenchymal stem cells for cartilage regeneration based on tetrahedral framework nucleic acid recruitment Biomaterials 278 121131

Yu H S, You Z F, Yan X J, Liu W, Nan Z R, Xing D, Huang C Y and Du Y N 2020 TGase-enhanced microtissue assembly in 3D-printed-template-scaffold (3D-MAPS) for large tissue defect reparation Adv. Healthcare Mater. 9 e2000531

Tamaddon M et al 2022 In vivo evaluation of additively manufactured multi-layered scaffold for the repair of large osteochondral defects Bio-Des. Manuf. 5 481–96

Xu T, Miszuk J M, Zhao Y, Sun H L and Fong H 2015 Electrospun polycaprolactone 3D nanofibrous scaffold with interconnected and hierarchically structured pores for bone tissue engineering Adv. Healthcare Mater. 4 2238–46

Hu S G, Meng Z J, Zhou J P, Li Y W, Su Y, Lei Q, Mao M, Qu X L, He J K and Wang W 2022 Enhanced attachment and collagen type I deposition of MC3T3-E1 cells via electrohydrodynamic printed sub-microscale fibrous architectures Int. J. Bioprinting 8 514

Yu C L, Guan G P, Glas S, Wang L, Li Z T and Turng L S 2021 A biomimetic basement membrane consisted of hybrid aligned nanofibers and microfibers with immobilized collagen IV and laminin for rapid endothelialization Bio-Des. Manuf. 4 171–89

Huang B Y, Aslan E, Jiang Z Y, Daskalakis E, Jiao M H, Aldalbahi A, Vyas C and Bártolo P 2020 Engineered dual-scale poly (ε-caprolactone) scaffolds using 3D printing and rotational electrospinning for bone tissue regeneration Addit. Manuf. 36 101452

Wang Z X, Wang H, Xiong J J, Li J H, Miao X M, Lan X Z, Liu X J, Wang W L, Cai N and Tang Y D 2021 Fabrication and in vitro evaluation of PCL/gelatin hierarchical scaffolds based on melt electrospinning writing and solution electrospinning for bone regeneration Mater. Sci. Eng. C 128 112287

Wang C J, Yang Y, Ji J Y, Fang Y C, Ouyang L L, Zhang L and Sun W 2022 3D-printed bioresorbable stent coated with dipyridamole-loaded nanofiber for restenosis prevention and endothelialization Int. J. Bioprinting 8 543

Oliveira S M, Silva T H, Reis R L and Mano J F 2013 Hierarchical fibrillar scaffolds obtained by non-conventional layer-by-layer electrostatic self-assembly Adv. Healthcare Mater. 2 422–7

Geng M R, Zhang Q Q, Gu J N, Yang J, Du H B, Jia Y T, Zhou X J and He C L 2021 Construction of a nanofiber network within 3D printed scaffolds for vascularized bone regeneration Biomater. Sci. 9 2631–46

Yu Y X, Hua S, Yang M K, Fu Z Z, Teng S S, Niu K R, Zhao Q H and Yi C Q 2016 Fabrication and characterization of electrospinning/3D printing bone tissue engineering scaffold RSC Adv. 6 110557–65

John J V, McCarthy A, Wang H J, Luo Z Y, Li H B, Wang Z X, Cheng F, Zhang Y S and Xie J W 2021 Freeze-casting with 3D-printed templates creates anisotropic microchannels and patterned macrochannels within biomimetic nanofiber aerogels for rapid cellular infiltration Adv. Healthcare Mater. 10 2100238

John J V, McCarthy A, Wang H J, Chen S X, Su Y J, Davis E, Li X W, Park J S, Reinhardt R A and Xie J W 2020 Engineering biomimetic nanofiber microspheres with tailored size, predesigned structure, and desired composition via gas bubble-mediated coaxial electrospray Small 16 1907393

Ha Y J, Ma X J, Li S K, Li T, Li Z H, Qian Y H, Shafiq M, Wang J W, Zhou X J and He C L 2022 Bone microenvironment-mimetic scaffolds with hierarchical microstructure for enhanced vascularization and bone regeneration Adv. Funct. Mater 32 2200011

Jiang S J et al 2022 Radially porous nanocomposite scaffolds with enhanced capability for guiding bone regeneration in vivo Adv. Funct. Mater. 32 2110931

Meng Z J, He J K, Cai Z H, Zhang M K, Zhang J L, Ling R and Li D C 2020 In-situ re-melting and re-solidification treatment of selective laser sintered polycaprolactone lattice scaffolds for improved filament quality and mechanical properties Biofabrication 12 035012

Gao H L, Wang Z Y, Cui C, Bao J Z, Zhu Y B, Xia J, Wen S M, Wu H A and Yu S H 2021 A highly compressible and stretchable carbon spring for smart vibration and magnetism sensors Adv. Mater. 33 2102724

Boda S K, Chen S X, Chu K, Kim H J and Xie J Q 2018 Electrospraying electrospun nanofiber segments into injectable microspheres for potential cell delivery ACS Appl. Mater. Interfaces 10 25069–79

Bidgoli M R, Alemzadeh I, Tamjid E, Khafaji M and Vossoughi M 2019 Fabrication of hierarchically porous silk fibroin-bioactive glass composite scaffold via indirect 3D printing: effect of particle size on physico-mechanical properties and in vitro cellular behavior Mater. Sci. Eng. C 103 109688

Meng Z J, He J K, Xia Z X and Li D C 2020 Fabrication of microfibrous PCL/MWCNTs scaffolds via melt-based electrohydrodynamic printing Mater. Lett. 278 128440

Bai G, Yuan P Y, Cai B L, Qiu X Y, Jin R H, Liu S Y, Li Y and Chen X 2019 Stimuli-responsive scaffold for breast cancer treatment combining accurate photothermal therapy and adipose tissue regeneration Adv. Funct. Mater. 29 1904401

Naderi N, Griffin M F, Mosahebi A, Butler P E and Seifalian A M 2020 Adipose derived stem cells and platelet rich plasma improve the tissue integration and angiogenesis of biodegradable scaffolds for soft tissue regeneration Mol. Biol. Rep. 47 2005–13

Liao H T, Chang K H, Jiang Y, Chen J P and Lee M Y 2011 Fabrication of tissue engineered PCL scaffold by selective laser-sintered machine for osteogeneisis of adipose-derived stem cells Virtual Phys. Prototyp. 6 57–60

An Y et al 2018 Autophagy promotes MSC-mediated vascularization in cutaneous wound healing via regulation of VEGF secretion Cell Death Discov. 9 58

Li L, Zhang Y, Lu H Y, Wang Y F, Xu J S, Zhu J X, Zhang C and Liu T X 2020 Cryopolymerization enables anisotropic polyaniline hybrid hydrogels with superelasticity and highly deformation-tolerant electrochemical energy storage Nat. Commun. 11 62

Seifert A, Gruber J, Gbureck U and Groll J 2021 Morphological control of freeze-structured scaffolds by selective temperature and material control in the ice-templating process Adv. Eng. Mater. 24 2100860

Caliari S R and Harley B A C 2011 The effect of anisotropic collagen-GAG scaffolds and growth factor supplementation on tendon cell recruitment, alignment, and metabolic activity Biomaterials 32 5330–40

Ma P X 2008 Biomimetic materials for tissue engineering Adv. Drug Deliv. Rev. 60 184–98

Yu C, Bianco J, Brown C, Fuetterer L, Watkins J F, Samani A and Flynn L E 2013 Porous decellularized adipose tissue foams for soft tissue regeneration Biomaterials 34 3290–302

Meng Z J, He J K, Cai Z H, Wang F P, Zhang J L, Wang L, Ling R and Li D C 2020 Design and additive manufacturing of flexible polycaprolactone scaffolds with highly-tunable mechanical properties for soft tissue engineering Mater. Des. 189 108508

Yeo M and Kim G 2020 Micro/nano-hierarchical scaffold fabricated using a cell electrospinning/3D printing process for co-culturing myoblasts and HUVECs to induce myoblast alignment and differentiation Acta Biomater. 107 102–14

Hu C, Chu C Y, Liu L, Wang C B, Jin S E, Yang R L, Rung S, Li J S, Qu Y L and Man Y 2021 Dissecting the microenvironment around biosynthetic scaffolds in murine skin wound healing Sci. Adv. 7 eabf0787

Lu K J, Qian Y, Gong J X, Zhu Z Y, Yin J, Ma L, Yu M F and Wang H M 2021 Biofabrication of aligned structures that guide cell orientation and applications in tissue engineering Bio-Des. Manuf. 4 258–77

Rossi E, Gerges I, Tocchio A, Tamplenizza M, Aprile P, Recordati C, Martello F, Martin I, Milani P and Lenardi C 2016 Biologically and mechanically driven design of an RGD-mimetic macroporous foam for adipose tissue engineering applications Biomaterials 104 65–77

Zhang J X, Liu Y Z, Chen Y T, Yuan L, Liu H, Wang J C, Liu Q R and Zhang Y 2020 Adipose-derived stem cells: current applications and future directions in the regeneration of multiple tissues Stem Cells Int. 2020 8810813

Chhaya M P, Melchels F P W, Holzapfel B M, Baldwin J G and Hutmacher D W 2015 Sustained regeneration of high-volume adipose tissue for breast reconstruction using computer aided design and biomanufacturing Biomaterials 52 551–60

Chhaya M P, Balmayor E R, Hutmacher D W and Schantz J T 2016 Transformation of breast reconstruction via additive biomanufacturing Sci. Rep. 6 28030

Cho W W, Kim B S, Ahn M, Ryu Y H, Ha D H, Kong J S, Rhie J W and Cho D W 2021 Flexible adipose-vascular tissue assembly using combinational 3D printing for volume-stable soft tissue reconstruction Adv. Healthcare Mater. 10 2001693

Zhang K X, Song L, Wang J, Yan S F, Li G F, Cui L and Yin J B 2017 Strategy for constructing vascularized adipose units in poly(L-glutamic acid) hydrogel porous scaffold through inducing in-situ formation of ASCs spheroids Acta Biomater. 51 246–57

Kato H, Mineda K, Eto H, Doi K, Kuno S, Kinoshita K, Kanayama K and Yoshimura K 2014 Degeneration, regeneration, and cicatrization after fat grafting: dynamic total tissue remodeling during the first 3 months Plast. Reconstr. Surg. 133 303e–13e

Xu T, Yao Q Q, Miszuk J M, Sanyour H J, Hong Z K, Sun H L and Fong H 2018 Tailoring weight ratio of PCL/PLA in electrospun three-dimensional nanofibrous scaffolds and the effect on osteogenic differentiation of stem cells Colloids Surf. B 171 31–39

Gao Q, Gu H B, Zhao P, Zhang C M, Cao M Y, Fu J Z and He Y 2018 Fabrication of electrospun nanofibrous scaffolds with 3D controllable geometric shapes Mater. Des. 157 159–69

Pati F, Ha D H, Jang J, Han H H, Rhie J W and Cho D W 2015 Biomimetic 3D tissue printing for soft tissue regeneration Biomaterials 62 164–75

Fang Y C, Ouyang L L, Zhang T, Wang C J, Lu B C and Sun W 2020 Optimizing bifurcated channels within an anisotropic scaffold for engineering vascularized oriented tissues Adv. Healthcare Mater. 9 2000782

Li Y, Lv S, Yuan H P, Ye G, Mu W B, Fu Y, Zhang X, Feng Z Y, He Y and Chen W 2021 Peripheral nerve regeneration with 3D printed bionic scaffolds loading neural crest stem cell derived Schwann cell progenitors Adv. Funct. Mater. 31 2010215

Mao M, He J K, Li Z, Han K and Li D C 2020 Multi-directional cellular alignment in 3D guided by electrohydrodynamically-printed microlattices Acta Biomater. 101 141–51

Liu X Z, Chen M M, Luo J C, Zhao H, Zhou X C, Gu Q L, Yang H L, Zhu X S, Cui W G and Shi Q 2021 Immunopolarization-regulated 3D printed-electrospun fibrous scaffolds for bone regeneration Biomaterials 276 121037

Embedding aligned nanofibrous architectures within 3D-printed polycaprolactone scaffolds for directed cellular infiltration and tissue regeneration

doi: 10.1088/2631-7990/acbd6c

Abstract

Keywords

通讯作者: 陈斌, bchen63@163.com

Article Metrics